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Clinical Microbiology Reviews logoLink to Clinical Microbiology Reviews
. 2004 Oct;17(4):863–893. doi: 10.1128/CMR.17.4.863-893.2004

Epidemiologic Background of Hand Hygiene and Evaluation of the Most Important Agents for Scrubs and Rubs

Günter Kampf 1,2,*, Axel Kramer 2
PMCID: PMC523567  PMID: 15489352

Abstract

The etiology of nosocomial infections, the frequency of contaminated hands with the different nosocomial pathogens, and the role of health care workers' hands during outbreaks suggest that a hand hygiene preparation should at least have activity against bacteria, yeasts, and coated viruses. The importance of efficacy in choosing the right hand hygiene product is reflected in the new Centers for Disease Control and Prevention guideline on hand hygiene (J. M. Boyce and D. Pittet, Morb. Mortal. Wkly. Rep. 51:1-45, 2002). The best antimicrobial efficacy can be achieved with ethanol (60 to 85%), isopropanol (60 to 80%), and n-propanol (60 to 80%). The activity is broad and immediate. Ethanol at high concentrations (e.g., 95%) is the most effective treatment against naked viruses, whereas n-propanol seems to be more effective against the resident bacterial flora. The combination of alcohols may have a synergistic effect. The antimicrobial efficacy of chlorhexidine (2 to 4%) and triclosan (1 to 2%) is both lower and slower. Additionally, both agents have a risk of bacterial resistance, which is higher for chlorhexidine than triclosan. Their activity is often supported by the mechanical removal of pathogens during hand washing. Taking the antimicrobial efficacy and the mechanical removal together, they are still less effective than the alcohols. Plain soap and water has the lowest efficacy of all. In the new Centers for Disease Control and Prevention guideline, promotion of alcohol-based hand rubs containing various emollients instead of irritating soaps and detergents is one strategy to reduce skin damage, dryness, and irritation. Irritant contact dermatitis is highest with preparations containing 4% chlorhexidine gluconate, less frequent with nonantimicrobial soaps and preparations containing lower concentrations of chlorhexidine gluconate, and lowest with well-formulated alcohol-based hand rubs containing emollients and other skin conditioners. Too few published data from comparative trials are available to reliably rank triclosan. Personnel should be reminded that it is neither necessary nor recommended to routinely wash hands after each application of an alcohol-based hand rub. Long-lasting improvement of compliance with hand hygiene protocols can be successful if an effective and accessible alcohol-based hand rub with a proven dermal tolerance and an excellent user acceptability is supplied, accompanied by education of health care workers and promotion of the use of the product.

INTRODUCTION

Nosocomial infections (NIs) remain a major global concern. Approximately 2 million NIs occur annually in the United States (232). Overall national prevalence rates have been described as ranging between 3.5 and 9.9% (160), but they vary significantly between departments, patient groups, types of surgical procedures, and the use of indwelling medical devices, etc. (20, 162). The most common NIs are urinary tract infections, lower respiratory tract infections, surgical-site infections, and primary septicemia (27, 159, 528, 532). They lead to additional days of treatment (146, 232, 411, 431, 605), increase the risk of death (27, 157), and increase treatment costs (217, 232, 234, 414, 431, 440, 460, 489, 605). The overall financial burden incurred by NIs has been estimated to be $4.5 billion per year in the United States alone (232). Approximately one-third of all NIs are regarded as preventable (193).

In 2002, a new Centers for Disease Control and Prevention (CDC) guideline for hand hygiene in health care settings, entitled Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force, was published (71). It provides health care workers with a review of data on hand washing and hand antisepsis in health care settings and provides specific recommendations to promote improved hand hygiene practices and reduce the transmission of pathogenic microorganisms to patients and personnel in health care settings. As a clinical guideline, its chief aim is to reduce the incidence of NIs by providing detailed recommendations on two main aspects of hand hygiene: (i) choice of the most appropriate agents for hand hygiene in terms of efficacy and dermal tolerance and (ii) different strategies to improve compliance in hand hygiene, including hand hygiene practices among health care workers, behavioral theories, and methods for reducing adverse effects of agents. Our review is intended to support the CDC guideline by presenting specific additional aspects of the various agents, such as a broader evaluation of the in vitro and in vivo efficacy in various test models and their mode of action, resistance potential, and effect on compliance in hand hygiene.

Hand hygiene has been considered to be the most important tool in NI control (403, 462) ever since Semmelweis observed its immense effect on the incidence of childbed fever (473). Health care workers have three opportunities for the postcontamination treatment of hands: (i) the social hand wash, which is the cleaning of hands with plain, nonmedicated bar or liquid soap and water for removal of dirt, soil, and various organic substances; (ii) the hygienic (Europe) or antiseptic (United States) hand wash, which is the cleaning of hands with antimicrobial or medicated soap and water (“scrub”); most antimicrobial soaps contain a single active agent and are usually available as liquid preparations; and (iii) the hygienic hand disinfection (Europe), which normally consists of the application of an alcohol-based hand rub into dry hands without water.

For the preoperative treatment of hands two options are available: (i) the surgical hand wash (Europe) or surgical hand scrub (United States) which is the cleaning of hands with antimicrobial soap and water; and (ii) the surgical hand disinfection (Europe), which is the application of an alcohol-based hand rub into dry hands without water.

Three main types of preparations can be used for the different procedures of hand hygiene. (i) The first is plain, nonmedicated soap (social hand wash). (ii) The second is medicated soap (antiseptic and surgical hand wash). The most commonly used agent is chlorhexidine, usually at a concentration of 4 or 2%. Triclosan can also be found in medicated soaps, usually at a concentration of 1%. Hexachlorophene has now been banned worldwide because of its high rate of dermal absorption and subsequent toxic effects, especially among newborns (84, 98). Levels of 0.1 to 0.6 ppm in blood were found among health care workers who regularly used a 3% hexachlorophene preparation for hand washing (323). These findings speak strongly against the topical use of this active agent. The Food and Drug Administration classifies this agent as not being generally recognized as safe and effective for use as an antiseptic hand wash (21). Hexachlorophene is therefore not included in this review. Other active agents such as povidone iodine have rarely been used for the postcontamination treatment of hands and therefore are also not addressed in this review. (iii) The final type is the alcohol-based hand rub (hygienic and surgical hand disinfection). This is a leave-on preparation and this applied to the skin without the use of water.

In addition, non-alcohol-based waterless antiseptic agents are available for use by health care workers. Some of these contain quaternary ammonium-type compounds. They were not discussed in the CDC hand hygiene guideline because there was insufficient evidence at the time to promote their use; therefore, they are not further evaluated here.

This review provides an in-depth comparison of the several options for hand hygiene, with the aim of further supporting the CDC guideline on hand hygiene.

TYPES OF SKIN FLORA

Three principal types of skin flora have been described. The resident and transient flora were already distinguished in 1938 (447, 470). In addition, the infectious flora was described, with species such as Staphylococcus aureus or beta-hemolytic streptococci, which are frequently isolated from abscesses, whitlows, paronychia, or infected eczema (475).

The resident flora consists of permanent inhabitants of the skin. They are found mainly on the surface of the skin and under the superficial cells of the stratum corneum (379). These bacteria are not regarded as pathogens on intact skin but may cause infections in sterile body cavities, in the eyes, or on nonintact skin (292). Resident skin bacteria survive longer on intact skin than do gram-negative transient species (325). The protective function of the resident flora, so-called colonization resistance, has been demonstrated in various in vitro and in vivo studies. Its purpose is twofold: microbial antagonism and the competition for nutrients in the ecosystem (12). Nevertheless, the interactions between bacteria and fungi on the skin are still inadequately understood. Many such interactions have been demonstrated experimentally. Their contribution—which is thought to be a major mechanism of preventing the adherence of pathogens—to the stability of the dermal ecosystem, however, remains unclear (375).

The dominant species is Staphylococcus epidermidis, which is found on almost every hand (311, 454, 522). The incidence of oxacillin resistance among isolates of S. epidermidis is up to 64.3% (311) and is higher among health care workers who have direct contact with patients than in those who do not (522). Other regular residents are Staphylococcus hominis and other coagulase-negative staphylococci, followed by coryneform bacteria such as propionibacteria, corynebacteria, dermabacteria, and micrococci (137, 315, 401). Among fungi, the most important genus of the resident skin flora is Pityrosporum (Malassezia) (201). Viruses are usually not resident on the skin but can proliferate within the living epidermis, where they may induce pathological changes (361).

Total counts of bacteria on the hands of medical staff have ranged from 3.9 × 104 to 4.6 × 106 (294, 309, 338, 447). Their number increases with the duration of clinical activities, on average by 16 cells per min (438). Some clinical situations are associated with a higher bacterial load on the hands of health care workers: direct contact with patients, respiratory tract care, contact with body fluids, and after being interrupted while caring for a patient (438). In general, however, it is difficult to clearly assign a specific risk of hand contamination to certain patient care activities. Nurses can contaminate their hands with 100 to 1,000 CFU of Klebsiella spp. during “clean activities” (81), while 10 to 600 CFU/ml can be found on nurses' hands after touching the groins of patients heavily contaminated with Proteus mirabilis (129). In intensive care units (ICU), the number of direct contacts between the hands of the health care workers and the patients is particularly high, leading to a higher risk of NI (148).

The transient skin flora consists of bacteria, fungi, and viruses that may be found on the skin only at times (447). They usually do not multiply on the skin, but they survive and occasionally multiply and cause disease (15). They may come from patients or inanimate surfaces. Between 4 and 16% of the hand surface is exposed by a single direct contact, and after 12 direct contacts, up to 40% of the hand surface may have been touched (74). The transmissibility of transient bacteria depends on the species, the number of bacteria on the hand, their survival on skin, and the dermal water content (230, 344, 418).

In addition, there is the temporary resident skin flora, which persists and multiplies for a limited period on the skin. The definition is more or less identical to that of transient skin flora, because the duration of residence on human skin is uncertain and variable but never permanent (5). In addition, the temporary resident skin flora often includes nosocomial bacteria and fungi (5, 201, 399, 400).

MICROBIAL AND VIRAL FLORAS OF HANDS AND THEIR EPIDEMIOLOGIC ROLE

Gram-Positive Bacteria

Role in NIs.

S. aureus is the most common gram-positive bacterium causing NIs (353, 533). Its frequency among all pathogens in NIs varies between 11.1 and 17.2% (265, 484, 493, 583). Methicillin resistance in S. aureus (MRSA) is increasing worldwide (113, 503, 578), leading not only to NIs but recently also to community-acquired infection. In 139 ICUs in Germany, 14.3% of all 1,535 NIs due to S. aureus have been caused by MRSA. This proportion is highest for urinary tract infections (26.4%), followed by primary septicemia (23.3%), and lower respiratory tract infection (12.9%) (161). The most common type of NI caused by S. aureus is the surgical-site infection (245, 259, 422).

Enterococcus spp. are isolated in up to 14.8% of patients with NI (484). The most common species are Enterococcus faecium and E. faecalis (385), which frequently cause urinary tract infections (533). The emergence of vancomycin resistance among enterococci (VRE) has led to an increased recognition of cross-transmission of VRE, including the role of health care workers' hands (29, 347).

Coagulase-negative staphylococci, such as S. epidermidis, mainly cause catheter-associated primary bloodstream infections. In ICUs, approximately one-third of all blood culture isolates from patients with nosocomial bloodstream infections were found to be coagulase-negative staphylococci (463, 533).

Frequency of colonized hands.

Colonization of health care workers' hands with S. aureus has been described to range between 10.5 and 78.3% (Table 1). Up to 24,000,000 cells can be found per hand (33). The colonization rate with S. aureus was higher among doctors (36%) than among nurses (18%), as was the bacterial density of S. aureus on the hands (21 and 5%, respectively, with more than 1,000 CFU per hand) (101). The carrier rate may be up to 28% if the health care worker contacts patients with an atopic dermatitis which is colonized by S. aureus (608, 609). MRSA has been isolated from the hands of up to 16.9% of health care workers. VRE can be found on the hands of up to 41% of health care workers (Table 1).

TABLE 1.

Contamination rates of health care workers' hands with nosocomial pathogens and their persistence on hands and inanimate surfacesa

Pathogen Contamination rate(s) of health care workers' hands (%) (references) Duration of persistence on hands (references) Duration of persistence on inanimate surfaces (references)
Acinetobacter spp. 3-15 (132, 335, 519) ≥150 min (33) 3 days-5 mo (166,233,387,393,596,598)
B. cereus 37 (569) Unknown Unknown
C. difficile 14-59 (362, 491) Unknown ≥24 h (vegetative cells), up to 5 mo (spores) (363)
E. coli Unknown 6-90 min (33, 151) 2 h-16 mo (3,111,190,350,376,393,509)
“Gram-negative bacteria” 21-86.1 (4, 7, 166, 187, 271, 302, 378) Unknown Unknown
Influenzavirus, parainfluenzavirus Unknown 10-15 min (25, 46) 12-48 h (46,72,433,614)
HAV Unknown Several hours (354, 355) 2 h-60 days (1,2,356)
HCV 8-23.8 (11) Unknown Unknown
Klebsiella spp. 17 (81) Up to 2 h (33, 81, 151, 514) 2 h-30 mo (111,190,376,393,509)
MRSA Up to 16.9 (378, 412, 542) Unknown 4 wk-7 mo (114,581)
P. vulgaris Unknown ≥30 min (33) 1-2 days (376)
Pseudomonas spp. 1.3-25 (53, 119, 144, 420, 607) 30-180 min (33, 119) 6 h-16 mo (111,178,190,393,509)
Rhinovirus Up to 65 (191, 457) Unknown 2 h-7 days (456,497)
Rotavirus 19.5-78.6 (490) Up to 260 min (22) 6-60 days (1, 2, 24)
Salmonella spp. Unknown ≤3 h (427) 6 h-4.2 yr (209, 376, 467)
S. marcescens 15.4-24 (90, 492) ≥30 min (33) 3 days-2 mo (111,376)
S. aureus 10.5-78.3 (90, 101, 179, 359, 378, 412, 546) ≥150 min (33) 4 wk-7 mo (190,394,509,581,582)
VRE Up to 41 (202) Up to 60 min (402) 5 days-4 mo (39,393,394,402,599)
“Yeasts,” including Candida spp. and Torulopsis glabrata 23-81 (90, 112, 221, 378, 541) 1 h (79, 564) 1-150 days (65,452,564)
a

Persistance of nosocomial pathogens on inanimate surfaces is important because of the high rate of acquisition of these pathogens on the hands after contact with environmental surfaces (58).

Role of hand colonization in cross-transmission.

Hand carriage of pathogens such as S. aureus, MRSA, or S. epidermidis has repeatedly been associated with different types of NI (Table 2) (212, 455). The analysis of outbreaks revealed that dermatitis on the hands of health care workers was a risk factor for colonization or for inadequate hand hygiene, resulting in various types of NI (Table 2).

TABLE 2.

Overview of NIs traced to the hands of an individual health care worker or another relevant point source and analysis of the main reason for transmission

Pathogen Type and no. of NIs Department Source Reason for transmission Reference
Adenovirus Epidemic keratoconjunctivitis, 126 Ophthalmology Infected doctor Carrier (hand) 235
C. tropicalis Surgical site infections, 8 Cardiothoracic surgery Surgical nurse Carrier (hand), use of nonmedicated soap before surgery due to intolerance of the antiseptic soap 226
HCV Hepatitis C, 5 Orthopedic and general surgery Infected anesthesist Wound on finger during incubation 469
K. aerogenes Urinary tract infections, 17 Urology Nurse Carrier (hand) 82
MRSA Diarrhea, 8 Orthopedic surgery Health care worker Carrier (nose and hands) 507
MRSA Surgical-site infections, 3 Pediatric cardiovascular surgery Surgeon Carrier (nose and hands) 595
MRSA Surgical-site infections, 5 Cardiac surgery Hand of assisting surgeon Dermatitis on hand of surgeon 589
S. liquefaciens Bloodstream infections, 15 Hemodialysis Contaminated medicated soap Transient hand carriage, leading to contamination of epoetin alpha 183
S. marcescens Septicemia, meningitis, pneumonia, 14 Neonatal ICU Contaminated triclosan-based liquid soap Use of soap, resulting in transient hand carriage 574
S. marcescens Septicemia, meningitis, 15 Neonatal ICU Contaminated brush Use of the brush, probably resulting in transient hand carriage 16
S. marcescens Pneumonia, septicemia, urinary tract infection, surgical-site infection, 83 11 different units Contaminated liquid soap Use of soap, resulting in transient hand carriage 492
S. marcescens Surgical-site infections, 5; septicemia, 2 Cardiovascular surgery Surgical nurse Highly contaminated nail cream 417
S. aureus Dermatitis exfoliativa, 42 Obstetrics Midwife Hand eczema 102
S. epidermidis Surgical-site infections with mediastinitis, 7 Cardiovascular surgery Hand of assisting surgeon Chronic dermatitis on hand of surgeon 292

Transmissibility of VRE has also been demonstrated. The hands and gloves of 44 health care workers were sampled after care of VRE-positive patients. Gloves were VRE positive for 17 of 44 healthcare workers, and hands were positive for 5 of 44, even though they had worn gloves (553). One health care worker was even VRE positive on the hands although the culture from the glove was negative (553).

Survival on hands and surfaces.

S. aureus can survive on hands for at least 150 min; VRE survives on hands or gloves for up to 60 min (Table 1). On inanimate surfaces, S. aureus and MRSA may survive for 7 months, with wild strains surviving longer than laboratory strains (Table 1). VRE may survive on surfaces for 4 months. The long survival on surfaces, together with the relatively short survival on hands, suggests that contaminated surfaces may well be the source of transient colonization despite negative hand cultures.

Gram-Negative Bacteria

Role in NIs.

Escherichia coli is the most common gram-negative bacterium, causing mainly urinary tract infections (265, 463). Pseudomonas aeruginosa is also very common, chiefly causing lower respiratory tract infections (265, 463). In the majority of cases, both types of infection are device associated (364, 463, 531) and are often found among patients in ICUs (260). Manual handling of devices such as urinary catheters, ventilation equipment, and suction tubes emphasizes the importance of the hands of health care workers in possible cross-transmission of gram-negative bacteria. Overall, gram-negative bacteria are found in up to 64% of all NIs (463).

Frequency of colonized hands.

Colonization rates of gram-negative bacteria on the hands of health care workers have been described as ranging from 21 to 86.1% (Table 1), with the highest rate being found in ICUs (271). The number of gram-negative bacteria per hand may be as large as 13,000,000 cells (33). The colonization may be long-lasting (302). Even in nursing homes, a rate of 76% has been described for nurses hands (610). Colonization with gram-negative bacteria is influenced by various factors. For example, it is higher before patient contact than after the work shift (187). Hands with artificial fingernails harbor gram-negative bacteria more often than those without (207). Higher colonization rates with gram-negative bacteria also occur during periods of higher ambient temperature and high air humidity (358).

Different species of gram-negative bacteria exhibit different colonization rates. For instance, the colonization rate is 3 to 15% for Acinetobacter baumannii, 1.3 to 25% for Pseudomonas spp., and 15.4 to 24% for Serratia marcescens (Table 1). Klebsiella spp. were found on the hands of 17% of the ICU staff sampled, with up to 10,000 bacteria per hand (81). Artificial fingernails have been associated with a higher risk for colonization with P. aeruginosa (144).

Role of hand colonization in cross-transmission.

Transient hand carriage of various gram-negative bacterial species has quite often been suspected to be responsible for cross-transmission during outbreaks resulting in various types of NI (155, 426, 514, 571). Most reports of cross-transmission of specific gram-negative bacteria come from critical-care areas, such as neonatal ICUs and burn units. Contaminated hands (Table 1), brushes, contaminated plain soap, and contaminated antiseptic soap have been associated with various types of NI, which were quite often caused by S. marcescens (Table 2).

Survival on hands and surfaces.

Most gram-negative bacteria survive on the hands for 1 h or more. Survival on inanimate surfaces has been reported to be different for the different gram-negative species, with most of them surviving for many months (Table 1). In general, gram-negative bacteria survive for longer on inanimate surfaces than on human skin (151).

Spore-Forming Bacteria

Role in NIs.

The main spore-forming bacterium causing NIs is Clostridium difficile. It is estimated that between 15 and 55% of all cases of nosocomial antibiotic-associated diarrhea are caused by C. difficile (40, 374, 567, 613). Patients with diarrhea caused by C. difficile have on average 3.6 additional hospital days attributable to the NI, which in the United States costs approximately $3,669 per case or $1.1 billion per year (289). The overall mortality is 15% (381). Extraintestinal manifestations are very uncommon (≤1%) (156). Patients can be contaminated from, for instance, the hands of hospital personnel and from inanimate surfaces (40).

Frequency of colonized hands.

In one study, the hands of 59% of 35 health care workers were C. difficile positive after direct contact with culture-positive patients. Colonization was found mainly in the subungual area (43%), on the fingertips (37%), on the palm (37%), and under rings (20%) (362). In another study, 14% of 73 health care worker were culture positive for C. difficile on their hands. The presence of C. difficile on the hands correlated with the density of environmental contamination (491). During a third outbreak, caused by Bacillus cereus in a neonatal ICU, 11 (37%) of 30 fingerprints from health care workers were positive for Bacillus spp. (569).

Role of hand colonization in cross-transmission.

Transmission of C. difficile in an endemic setting on a general medical ward has been shown to occur in 21% of patients, with 37% of them suffering from diarrhea (362). An outbreak of necrotizing enterocolitis among neonates was associated with clostridial hand carriage in four of seven health care workers (173). Another spore-forming bacterium has been described as well: B. cereus was transmitted to the umbilicus in 49% of newborns on a maternity ward; the hands of 15% of the health care workers were found to be culture positive (62).

Survival on hands and surfaces.

Vegetative cells of C. difficile can survive for at least 24 h on inanimate surfaces, and spores survive for up to 5 months (Table 1).

Fungi

Role in NIs.

Fungi are less commonly found than bacteria as the causative agent of NIs, but their frequency and importance are increasing (216, 502, 527). In Germany and New Zealand, 6% of all NIs were caused by fungi (397, 484). In Spain, the overall rate was found to be 2.4% in 1990 and 3.2% in 1999, indicating a higher clinical relevance for NIs in the more recent study (26). In the United States, an increase in isolation of yeasts from 7.6 to 10.6% has been noted over a period of 10 years in patients with NIs (593). The most important fungus with respect to NIs is Candida albicans. Fungi may cause septicemia, urinary tract infections, or surgical-site infections (463, 500). Device-associated bloodstream infections caused by Candida spp. have become more common among critically ill patients in the last decades (89, 128, 163, 342); the contribution of non-albicans Candida spp. is increasingly significant (216). It has also been reported that 21% of all urinary tract infections among ICU patients are caused by C. albicans (463).

Frequency of colonized hands.

In an ICU, 67 (46%) of the hands of 146 health care workers were colonized with a yeast. The most common species were Candida and Rhodotorula spp. Respiratory therapists were found to have the highest colonization rate (69%) (221). In another study of nurses and other hospital staff, 75% of the nurses and 81% of the other hospital staff were colonized with a yeast (541). In a long-term-care facility, 41% of 42 health care workers were found to have Candida spp. on their hands (378). Yeasts quite often also colonize artificial fingernails (207). Acquisition of C. albicans on the hands of health care workers immediately after attending systemically infected patients was reported to occur in 2 of 17 nurses (79).

Role of hand colonization in cross-transmission.

Only a few studies are found in the literature which demonstrate the role of hands in cross-transmission (Table 2), sometimes despite negative hand cultures (572). The analysis of an outbreak revealed that caring for a patient who is colonized with Candida parapsilosis can lead to positive hand cultures and finally to severe infections or colonization among patients (501). The transmissibility of yeasts from hand to hand is high (Table 3).

TABLE 3.

Transmissibility of nosocomial pathogens from contaminated hands

Type of pathogen Contact time (s) Target Transmission rate (%) Reference
C. albicans Unknown Hands 69 452
Feline calicivirus 10 Food 18-46 60
Steel surface 13
HAV 10 Lettuce 9.2 59
HSV-1 Unknown Hands 100 (moist skin), 60 (dry skin) 41
Rhinovirus 10 Hands 71 191
Rotavirus 10 Hands 6.6 22
Salmonella spp. 5 Meat 16 (inoculum of 7 cells per fingertip), 100 (inoculum of ≥600 cells per fingertip) 427

Survival on hands and surfaces.

On fingertips, only 20% of viable cells of C. albicans and C. parapsilosis remain detectable after 1 h (79, 564). Candida spp. can survive on surfaces for up to 150 days (452, 564). During this period of survival, most yeast cells die within the first few minutes (452).

Viruses

Role in NIs.

Viruses account for approximately 5% of all NIs. On pediatric wards, the proportion is higher at 23% (6). Five main groups of viruses have been identified with respect to their nosocomial transmission: blood-borne viruses (e.g., hepatitis B virus [HBV], hepatitis C virus [HCV], and human immunodeficiency virus [HIV]), respiratory route viruses (e.g., respiratory syncytial virus [RSV], influenza virus, rhinovirus, coronavirus, and adenovirus), fecal-oral route viruses (e.g., rotavirus, small round structured viruses [noroviruses], enteroviruses, and hepatitis A virus [HAV]), herpesviruses obtained from direct contact with skin, mucous membranes, or wounds (e.g., herpes simplex viruses, varicella zoster virus, cytomegalovirus, and Epstein-Barr virus), and exotic viruses such as viral hemorrhagic fever viruses (Ebola virus, Marburg virus, Lassa fever virus, and Congo Crimean hemorrhagic fever virus) and rabies virus (8). The fingers, especially the pads and tips, are the most likely areas to come into contact with viruses while touching infected people and their bodily substances as well as other contaminated materials (499, 576).

Frequency of contaminated hands.

The risk of direct contact with blood and thereby with blood-borne viruses is variable. In general, it must be assumed that a health care worker wears protective gloves if contact with blood is expected. However, there are still clinical situations in which contamination with blood is unexpected. Health care workers in invasive radiology have blood contact in 3% of clinical activities, surgeons have blood contact in 50%, and midwives have blood contact in 71% (48). Surgical gloves should protect from direct contact with blood, but perforations are found on average in 17% of gloves, which correlates with the detection of blood under surgical gloves in 13% of surgeons (392). Perforations in most gloves (83%) remain undetected by the surgeon (557). Up to 82.5% of protective gloves have invisible perforations (276). In an acute viremic state, HBV may be present in blood at a concentration of 5 × 108 IU per ml of blood (623). A 1-μl volume of blood, which is hardly visible on a hand, may still contain 500 IU of HBV. For HCV, a concentration of 104 to 107 IU was found in blood (105). Virus detection on the hands has been investigated in a few studies. In a dialysis unit, 23.8% of samples obtained from health care workers' hands were positive for HCV RNA after treatment of HCV-positive patients despite the use of standard precautions, whereas the rate was 8% after treatment of HCV-negative patients (11).

Viruses from the respiratory tract are often found on hands, e.g., rhinoviruses in up to 65% from persons with a common cold (191, 457). Adenovirus has been found on the hands of healthcare workers during outbreaks of keratoconjunctivitis (380) and was isolated from the hands of 46% of patients with epidemic keratoconjunctivitis (35), which emphasizes the potential of virus transfer to hospital personnel through casual hand contact. No data were available regarding the detection of severe acute respiratory syndrome (SARS) virus on hands during the outbreaks in Asia and Canada in 2003.

Rotaviruses can be found on the hands in up to 78.6% of individuals sampled (Table 1) and also on surfaces with frequent hand contact, e.g., TV sets, toys, and patient charts (9). At the peak of a bout of rotavirus gastroenteritis, every gram of feces may contain more than 107 to 108 infectious viral particles (590).

Cytomegalovirus has been isolated from the hands of day care workers (224), but exotic viruses such as hemorrhagic fever viruses have to date not been detected on health care workers' hands.

Role of hand colonization in cross-transmission.

Hands play a major role especially in the transmission of blood-borne, fecal, and respiratory tract viruses. The transmission of some viruses from the hands of health care workers has been described (Table 2). In addition, transient hand carriage is associated with the transmission of many viruses, such as rhinovirus (99, 191), RSV (194, 488), astrovirus (136), and cytomegalovirus (109). For the SARS virus, a similar correlation has been described, since hand hygiene was found to be the second most effective measure to prevent cross-transmission of the SARS virus in a hospital (510). Most viruses are easily transmitted from hand to hand, food, or surfaces (Table 3).

Persistence of infectivity on hands and surfaces.

Persistance of viruses on the hands has been investigated mainly for fecal and respiratory tract viruses. Artificial contamination of hands with HAV led to an immediate-recovery rate of 70.5% (59). HAV persisted for several hours on human hands (354, 355). With poliovirus, the immediate-recovery rate was 22% but the whole inoculum was recovered after 150 min, indicating an almost complete persistence of poliovirus on hands (505). Rotavirus has been described as persisting on hands for up to 260 min, with 57% recovery after 20 min, 42.6% recovery after 60 min, and 7.1% recovery after 260 min (22). It can be transferred from contaminated hands to clean hands, with 6.6% of the viral contamination transferred 20 min after contamination (Table 3), and 2.8% of the viral contamination transferred 60 min after contamination (22). Rotavirus has been described to persist better on hands than rhinovirus or parainfluenzavirus (24).

Many enveloped viruses such as influenza virus, parainfluenza virus (Table 1), and cytomegalovirus (139) may survive on the hands for 10 to 15 min or even up to 2 h (herpes simplex virus type 1 [Table 1]). Adenoviruses have been described to persist on human skin for many hours (499).

Only a few studies of the persistence of viruses on surfaces have been performed. Rotavirus and HAV can persist for up to 60 days (Table 1) depending on the room temperature, air humidity, and type of surface (495). HIV remains infective on surfaces for up to 7 days, depending on the inoculum and the type of preparation (cell-associated virus or cell-free virus). HIV obtained from clinical specimens remains infective for a few days (568). Influenza A virus may persist on steel for up to 48 h; on other materials, such as paper or handkerchiefs, the virus persists for up to 12 h (46). Rhinovirus may persist for up to 7 days (Table 1).

MINIMUM SPECTRUM OF ANTIMICROBIAL ACTIVITY

The new CDC guideline on hand hygiene does not suggest a specific minimum spectrum of antimicrobial activity of a suitable hand hygiene agent (71). However, it can be derived from the etiology of NIs as well as the data on the skin flora of the hands of health care workers and their role in the transmission of nosocomial pathogens (Table 4). A procedure for the postcontamination treatment of hands must have at least bactericidal, fungicidal (yeasts), and virucidal (coated viruses) activity.

TABLE 4.

Spectrum of antimicrobial activity of procedures for hand hygiene derived from the etiology of NIs, data on the transient flora of health care workers' hands, and their role in the transmission of nosocomial pathogens

Type of antimicrobial activity Required activity Optional activitya
Bactericidal +
Mycobactericidal +
Sporicidal +
Fungicidal (yeasts) +
Fungicidal +
Virucidal (enveloped viruses) +
Virucidal (including nonenveloped viruses) +
a

May be relevant in special patient care or during outbreaks.

The spectrum of activity can be substantiated in suspension tests (474). In principle, suspension tests are suitable to substantiate the spectrum of antimicrobial activity (474). The suggested activity against coated viruses is based on the frequent contamination of health care workers' hands with blood during routine patient care and thereby possibly with blood-borne viruses, such as HCV or HIV, where neither patients nor health care workers can be protected by vaccination. The contamination of hands with blood may not be visible but may still be infective with HCV or HIV for the health care worker or the next patient (123). That is why activity against coated viruses should be included in the minimum spectrum of activity for an active agent for hand hygiene. Uncoated viruses, however, are usually spread from patients with infective gastroenteritis (e.g., caused by noroviruses or rotaviruses), upper and lower respiratory tract infections, or keratoconjunctivitis (e.g., caused by adenoviruses). These infections often have typical and visible symptoms. The activity against uncoated viruses can be restricted to a specific clinical area, e.g., in ophthalmology (adenovirus), pediatrics (rotavirus), or oncology (parvovirus) or to outbreaks of specific infectious diseases caused by uncoated viruses. Additional activity against the whole spectrum of fungi (including molds), mycobacteria, and bacterial spores may be relevant in special patient care situations (e.g., in bone-marrow transplant units) or during outbreaks. A procedure for the preoperative treatment of hands should be at least bactericidally and fungicidally (yeasts) effective, since the hands of most health care workers' hands carry yeasts and since surgical-site infections have also been associated with hand carriage of yeasts during an outbreak.

AGENTS FOR REDUCTION OF THE NUMBERS OF PATHOGENS ON HANDS

Nonmedicated Soap (Social Hand Wash)

Normally, nonmedicated soaps are detergent-based products. Those based on esterified fatty acids and sodium or potassium hydroxide are less skin compatible (Table 5). They are available in various forms including bar soaps, tissue, leaflet, and liquid preparations. This cleaning activity can be attributed to the detergent properties.

TABLE 5.

Effect of alkali- and detergent-based nonmedicated soaps on human skina

Type of effect Effect observed with:
Alkaline-based soap Detergent-based soap
Formation of lime soaps Yes No
Swelling Substantial Small
Dehydration Moderate Moderate to strong
Degreasing Pronounced Pronounced, depending on the amount of detergent
pH shift to alkaline Substantial Preventable
Neutralization capacity Noticeably retarded Somewhat retarded
Regeneration of skin pH Strongly impaired Slightly impaired
Surfaction No Possible
a

Reprinted from reference 283 with permission of the publisher.

Effect on microorganisms and viruses. (i) Spectrum of activity.

Nonmedicated soaps do not contain any active ingredient with an antimicrobial activity apart from preservatives. That is why in vitro data on the antimicrobial activity of nonmedicated soap rarely exist. The first experiments with soft alkaline soap were carried out by Robert Koch. He found out that multiplication of the vegetative cells of Bacillus anthracis was completely (dilution of 1:1,000) or partly (dilution of 1:5,000) inhibited (273). A more recent study described a fungistatic effect of a tenside-based soap at dilutions between 1:64 and 1:1,000 against Trichosporon cutaneum. C. albicans. Trichophyton rubrum. Trichophyton schönleinii. Microsporum audouinii, and Microsporum canis (277). With one plain soap, even limited fungicidal activity was described and largely explained by the presence of preservatives (603).

(ii) Testing under practical conditions.

The use of plain soap and water reduces the numbers of microorganisms and viruses by mechanical removal of loosely adherent microorganisms from the hands. Many studies are available which address the reduction of the transient hand flora. The most common type of artificial contamination of hands for test purposes in the United States is S. marcescens (21), whereas E. coli is the main contaminant used in Europe (115). Regarding the transient flora, a reduction between 0.5 and 2.8 log10 units can be found within 1 min for E. coli (Table 6). Other types of artificial contamination have been used as well, such as VRE, rotavirus, Klebsiella spp., or spores of Bacillus atrophaeus. A simple hand wash still leads to a mean reduction of up to 2.4 log10 units within 1 min (Table 7). There is basically no effect on resident hand flora after a 2-min hand wash; after a 5-min hand wash, a reduction of 0.4 log10 unit was found, and after 3 h of wearing gloves, no reduction at all was observed (Table 8).

TABLE 6.

Effect of a simple hand wash with water alone on various types of artificial transient hand flora

Microorganism Duration of hand wash Mean removal rate (log10) Reference
E. coli 10 s 1.0 23
1 min 2.99 377
2 min 3.08 377
4 min 3.39-3.67 377
Klebsiella spp. 20 s 1.7 81
VRE 5 s 0 402
30 s 0 402
Rotavirus 10 s 0.79 23
30 s 1.26-1.57 47
TABLE 7.

Effect of a simple hand wash with plain soap and water on various types of artificial transient hand flora

Microorganism Duration of hand wash Mean removal rate (log10) Reference(s)
E. coli 10 s 0.5 23
15 s 0.6-1.1 406
30 s 1.37-3 34, 326, 330
1 min 2.6-3.23 257, 377, 478, 480
2 min 3.27 377
P. aeruginosa 30 s 2-3 330
Klebsiella spp. 20 s 1.7 81
S. aureus 30 s 0.52-3 34, 318, 330
S. saprophyticus 30 s 2.49 34
Rotavirus 10 s 0.14 23
30 s 1.17-1.19 47
C. difficile 10 s 2.0-2.4 57
B. atrophaeus 10 s 2.4 594
30 s 2.3 594
60 s 2.1 594
TABLE 8.

Effect of various agents for hand hygiene on the resident hand flora

Type of agent Concn (%) Duration of treatment (min) Mean removal rate (log10) Reference(s)
Plain soap NA 2 −0.05 36
NA 3 0.3-0.57 96
NA 5 0.3-0.4 208, 305, 326, 471
Chlorhexidine 4 2 0.35-1.0 36, 317, 329
4 3 0.68-1.75 96, 218, 341, 471, 472
4 5 0.9-1.6 49, 305, 404, 471
4 6 1.2 153
4 10 2.29 404
Triclosan 1 5 0.6 305
2 2 0.3 36
2 5 0.8 49
Ethanol 70 2 1.0 328
70 3 1.32 326
80 2 1.5 475
85 3 2.1-2.5 251
95 2 2.1 317, 320
Isopropanol 60 5 1.7 472
70 0.5 1.5 36
70 1 0.7-0.8 475
70 2 1.2-1.65 36, 328
70 3 1.5-2.0 475
70 5 2.1-2.4 475
80 3 2.3 483
90 3 2.4 483
n-propanol 60 1 1.1 475
60 3 0.8-2.9 213, 240, 251, 341
60 5 2.05-2.9 208, 213, 471, 479
a

NA, not applicable.

(iii) In-use tests.

The effect of a social hand wash “in real life” has also been studied. Among 224 healthy homemakers, a single hand wash had little impact on microbial counts (mean log counts before hand wash, 5.72 ± 0.99; mean log counts after hand wash, 5.69 ± 1.04) (307). In a study with 11 volunteers who washed their hands for 15 s with water alone 24 times per day for a total of 5 days, a slight increase of the bacterial counts was observed (mean log bacterial counts: prewash, 4.91 ± 0.46; postwash, 5.12 ± 0.44); when bar soap was used, a similar result was found (mean log bacterial counts: prewash, 4.81 ± 0.46; postwash, 5.07 ± 0.47) (299). Other authors, too, have found paradoxical increases in bacterial counts on the skin after hand washing with plain soap (299, 371, 611). In contrast, another study showed that a 5-min hand wash with regular bar soap reduced the resident hand flora by 0.33 log10 units (326). The use of a nonmedicated soap by a surgical nurse for the preoperative treatment of hands even led to eight cases of surgical-site infection after cardiac surgery, which underscores the limited efficacy of nonmedicated soap (226).

Some studies have examined only microorganisms that are left on the hands after a hand wash. Washing hands with soap and water has been described to be ineffective in eliminating adenovirus from the culture-positive hands of a physician and patients, indicating that mechanical removal was incomplete (235). Transient gram-negative bacteria remained on the hands of health care workers in 10 of 10 cases despite five successive hand washes with soap and water (187). Furthermore, transmission of gram-negative bacteria from hands has been shown to occur 11 of 12 cases when a simple hand wash is carried out (129).

(iv) Risk of contamination by a simple hand wash.

One risk of using soap and water is the contamination of hands by the washing process per se. This has been reported for P. aeruginosa (143). A possible source is the sink itself, when splashes of contaminated water come in contact with the hand of the health care worker (119). The reason is that the microorganisms are not killed during the hand wash but only removed and distributed in the immediate surroundings of the person, including the clothes. Nonmedicated soaps may also become contaminated and lead to colonization of the hands of personnel and to NIs, e.g., with S. marcescens (492) or Serratia liquefaciens (183).

Although the data involving nonmedicated soap suggest that a simple hand wash has some effect on the transient hand flora, it must be borne in mind that, in reality, a simple hand wash often does not last longer than 10 s (121, 145, 176, 177, 180, 300, 334, 450, 552).

Effect on human skin.

Each hand wash detrimentally alters the water-lipid layer of the superficial skin, resulting in a loss of various protective agents such as amino acids and antimicrobial protective factors. Regeneration of the protective film may be insufficient if many hand washes are carried out in a row. This may lead to damage of the barrier function of the stratum corneum by inhingement of intercellular putty substances. The transepidermal water loss (TEWL) increases, and the skin becomes more permeable for toxic agents. At the same time, the superficial skin cells dry out, resulting in dehiscence of the stratum corneum, initially on the microscopic level and in due course on the macroscopic level (280).

The incidence with which simple soaps and detergents affect the condition of the skin of health care workers' hands varies considerably (407). For years, natural soaps that have high pH values were thought to be more irritating to the skin than synthetic detergents with neutral or acidic pHs. However, subsequent studies have found that pH is less important than other product characteristics as a cause of skin irritation (200). In some studies, plain soaps have caused less skin irritation than synthetic detergents, while in others, plain bar soap caused greater skin irritation than did a synthetic antimicrobial-containing detergent (299, 565). Synthetic detergents also vary in their propensity to cause skin irritation (200, 407). The incidence of detergent-related-irritant contact dermatitis is affected by various factors: the concentration of the compound, the type of detergent (anionic, cationic, amphoteric, or nonionic) and its quantity, the refattening, the vehicle, the time of exposure, and area exposed (50, 133, 283, 565). For example, it has been shown in vivo that higher concentrations of sodium lauryl sulfate (a detergent) caused greater skin irritation than lower concentrations did (133). In addition, anionic detergents are known to cause greater skin irritation than amphoteric or nonionic detergents (565).

Another factor is the temperature of the water that is used for the hand wash. Hot water leads to greater skin irritation, as reflected by in vivo measurements of TEWL and in vitro measurements of the penetration of detergent through the skin (50, 133, 405). This is explained by an increased penetration of detergents into the epidermis (405). In addition, scaling of the skin is greater when hands are washed with hot water (50). Only skin hydration does not appear to be affected by higher water temperatures (50, 405).

Frequent hand washing induces irritative contact dermatitis (ICD) and dry skin (70, 275, 525, 611), which may become colonized with nosocomial pathogens. ICD can be found in 18.3% of nursing staff in hospitals and is a major occupational health concern (523). A single hand wash already significantly reduces the dermal sebum content; the reduction lasts for 1 h. Skin hydration drops at the same time (280). If hands are washed four times within 1 h, the skin does not recover to its normal state within this period (337). In a study with 52 volunteers who washed their hands 24 times per day for a total of 5 days, a significant increase of the TEWL was observed, indicating that the skin barrier function is impaired (299). The prevalence of ICD caused by hand washing with antimicrobial soaps (detergents) is related to the factors listed above (540). The hardness of water may also affect the incidence of ICD due to frequent hand washing (591).

In summary, plain soap has basically no antimicrobial activity. A simple hand wash can reduce transient bacteria by 0.5 to 3 log10 units but has no real effect on the resident hand flora. The dermal tolerance is rather poor (Table 9).

TABLE 9.

Comprehensive evaluation of the most important agents for hand hygienea

Criterion for evaluation Effect for:
Plain soap (hand wash) Chlorhexidine (2-4%) (hand wash) Triclosan (1-2%) (hand wash) Ethanol (60-85%) (hand rub) Isopropanol (60-80%) (hand rub) n-Propanol (60-80%) (hand rub)
Spectrum of activity
    Bacteria ++ ++ +++ +++ +++
    Mycobacteria (+) Unknown +++ +++ +++
    Bacterial spores
    Yeasts ++ ++ +++ +++ +++
    Dermatophytes + ++ Unknown Unknown
    Coated viruses ++ Unknown +++ +++ +++
    Uncoated virusesb + Unknown +c (+)d (+)d
Effect on hand flora (mean log10 reduction)
    Transient bacteria (≤1 min) 0.5-3 2.1-3 2.8 2.6-4.5 4.0-6.81 4.3-5.8
    Resident bacteria (≤3 min) ≤0.4 0.35-1.75 0.29-0.8 2.4 1.5-2.4 2.0-2.9
Potential for acquired bacterial resistance Moderate Low None None None
Effect on skin
    Skin hydration Decrease Decrease Decrease No change No change No change
    Skin barrier Impaired Impaired Impaired No change No change No change
    Skin irritation Likely Likely Possible Very uncommon Very uncommon Very uncommon
    Allergy Uncommon Possible Uncommon Extremely uncommone None None
Effect on compliance with hand hygiene (↓) (↓) (↓) (↑)
a

+++, effective within 30 s; ++, effective within 2 min; +, effective in >2 min; (+), partially effective; −, not effective.

b

Poliovirus and adenovirus, test viruses of prEN 14476.

c

Ethanol at 95% has virucidal activity within 2 min.

d

Results largely dependent on the test virus.

e

Individual cases, possibly due to impurities.

Chlorhexidine

Chlorhexidine is a cationic biguanide (485) and was first established as an antimicrobial agent in 1954 (104). It exists as acetate (diacetate), gluconate, and hydrochloride salts (485). Chlorhexidine gluconate is commonly used either at 0.5 to 0.75% in aqueous solution or in some detergent preparations or at 2 to 4% in other detergent preparations (327, 328). Its activity is greatly reduced in the presence of organic matter (485), natural corks (321), and hand creams containing anionic emulsifying agents (586). Inactivation of chlorhexidine may result in contamination of solutions containing 0.1% chlorhexidine, e.g., with Pseudomonas spp. (78).

The main target is the bacterial cytoplasmic membrane (360, 464). After chlorhexidine has caused extensive damage to the cytoplasmic inner membrane, precipitation or coagulation of protein and nucleic acids occurs (487). Damage also occurs to the outer membrane in gram-negative bacteria and the cell wall in gram-positive cells (131, 142, 227, 228, 236). Chlorhexidine also damages the cytoplasmic membrane of yeasts (588) and prevents the outgrowth, but not the germination, of bacterial spores (511). If chlorhexidine is hydrolyzed, small amounts of carcinogenic para-chloraniline may develop (87); this chemical has been found even in manufactured chlorhexidine solutions (274). At temperatures above 70°C, chlorhexidine is not stable and may degrade to para-chloraniline (171). An upper limit for para-chloraniline has been set in the British Pharmacopoeia at 0.25 mg per 100 mg of chlorhexidine (17).

Effect on microorganisms and viruses. (i) Spectrum of activity.

The antimicrobial activity of chlorhexidine is dependent on its concentration. At lower concentrations, chlorhexidine has a bacteriostatic effect against most gram-positive bacteria (e.g., at 1 μg/ml), many gram-negative bacteria (e.g., at 2 to 2.5 μg/ml) (100, 195), and bacterial spores (513). At chlorhexidine concentrations of 20 μg/ml or more, a bactericidal effect can be expected as well as activity against yeasts (487). The actual effective concentration against Burkholderia cepacia and S. aureus varies with different supplements from 0.004 to 0.4% (factor 100), and the actual killing time also varies with different supplements (phenylethanol or edetate disodium) from <15 min to >360 min (465). In most studies, concentrations for rapid inactivation are well in excess of MICs, e.g., for S. aureus (103), E. coli. Vibrio cholerae (237), and yeasts (214). When used in a liquid soap, chlorhexidine usually has a concentration of 4% and exhibits a bactericidal activity against various gram-negative (130) and gram-positive (249) bacteria. In some comparative studies using suspension tests chlorhexidine (4%) was found to be less effective against MRSA than against methicillin-susceptible S. aureus, which has raised concerns about the suitability of the active agent in the prevention of transmission of MRSA (93, 192, 249). This concern has been confirmed with enterococci. Against Enterococcus species and VRE, chlorhexidine (4%) was found to be essentially ineffective in suspension tests if neutralization of residual activity is excluded (247). In a comparison with a nonmedicated hand wash product, a chlorhexidine-based scrub yielded a lower reduction of different antibiotic-resistant test bacteria such as MRSA, VRE, or high-level gentamicin-resistant enterococci (175). Chlorhexidine has no sporicidal activity (513). The data on mycobactericidal activity are not unambiguous but do indicate the relevance of a threshold concentration of chlorhexidine. In one report, 4% chlorhexidine was described as having very good activity against Mycobacterium smegmatis (reduction of >6 log10 units within 1 min) (54), whereas another study with Mycobacterium tuberculosis suggested a low activity of 4% chlorhexidine (reduction of <3 log10 units within 1 min) (55). Chlorhexidine at 1.5% did not reveal sufficient activity against Mycobacterium bovis (56), and chlorhexidine at 0.5% had no activity against Mycobacterium avium. Mycobacterium kansasii, or M. tuberculosis within 120 min (466).

Against dermatophytes such as Trichophyton mentagrophytes, chlorhexidine (1.5%) has been described as having no activity (56).

Antiviral activity has been described as good against most enveloped viruses, such as HIV, cytomegalovirus, influenza virus, RSV, and herpes simplex virus (284, 441), but the virucidal activity of chlorhexidine against naked viruses such as rotavirus, adenovirus, or enteroviruses is low (391, 498).

In comparison to other active agents, chlorhexidine has been described to be less effective in vitro against various nosocomial pathogens than is benzalkonium chloride or povidone iodine (517).

Overall, chlorhexidine seems to have good residual activity (13, 34, 305, 328, 423, 468, 476), but the residual activity must be assessed with caution. It may be false positive due to insufficient neutralization of chlorhexidine in the test design, leading to bacteriostatic concentrations beyond the actual exposure time. Significant difficulties in effective neutralization in in vitro tests have been described, and may yield false-positive activity data for this active agent (246, 516, 517, 600). In addition, the clinical benefit of such a residual effect has never been shown.

(ii) Testing under practical conditions.

A 1-min hand wash with soap containing 4% chlorhexidine has been reported to lead to a mean reduction of E. coli of 3.08 log10 units on artificially contaminated hands (478). In a study with 52 volunteers who washed their hands 24 times per day for a total of 5 days, a significant decrease in the number of resident skin bacteria was observed with a 4% chlorhexidine liquid soap (mean reduction of 0.76 log10 unit) compared to nonmedicated bar soap (mean increase of 0.21 log10 unit) and a povidone-iodine soap (mean reduction of 0.32 log10 unit) (299). Under practical conditions with hands artificially contaminated by MRSA, chlorhexidine-based liquid soap was equally effective as simple soap (188, 220). A similar result was reported after contamination of hands with S. aureus (577). A reduction of 2.1 to 3 log10 units was found on hands contaminated with Klebsiella spp. after a 20-s hand wash with a soap based on 4% chlorhexidine (81). If hands were contaminated with rotavirus and treated with chlorhexidine soap for 10 s, the number of test viruses was reduced by 86.9%, which was significantly lower than the reductions achieved with 70% ethanol (99.8%) and 70% isopropanol (99.8%) (23). Treatment with 4% chlorhexidine soap for 30 s on hands contaminated with rotavirus leads to a similar effect of only 0.27 to 0.5 log10 unit (47). Under practical conditions and in terms of removal rate from hands, the efficacy against bacterial spores (e.g., B. atrophaeus) of an antiseptic liquid soap based on chlorhexidine was similar to that of nonmedicated soap, indicating that within 10 s or 60 s, chlorhexidine does not exhibit a significant sporicidal activity (57, 594). The effect of 4% chlorhexidine on the resident hand flora was found to be a reduction of between 0.35 and 2.29 log10 units, depending on the application time (Table 8).

(iii) In-use tests.

The in-use studies yield a heterogeneous picture of the efficacy of chlorhexidine. One of the first studies with chlorhexidine was performed in 1955. A hand cream containing 1% chlorhexidine was rubbed into dry hands and led to a substantial reduction is the number of resident skin bacteria after 30 min (386). In another clinical study, 74 health care workers evaluated plain soap and a liquid soap based on 4% chlorhexidine over 4 months in a neurosurgical unit and a vascular surgery ward. Overall hand contamination was found to be significantly lower after the use of plain soap (mean number of CFU, 125) than after the use of chlorhexidine (mean number of CFU, 150) (343). A hand wash with 4% chlorhexidine was reported to be more effective on the total bacterial count under clinical conditions than was a 1% triclosan hand wash (140). In a prospective crossover study over 4 months with plain soap and a 4% chlorhexidine soap among health care workers in two surgical units, plain soap was found to be significantly more effective than chlorhexidine in reducing bacterial counts from the hands of health care workers (343). After contamination of hands with Klebsiella spp., a 98% reduction was described in 19 of 23 experiments in which a soap based on 4% chlorhexidine was used (81); this is an almost 2 log10 unit reduction. Chlorhexidine failed to eliminate MRSA from the hands (140). In contrast, gram-negative bacteria were more likely to be eliminated after the use of chlorhexidine (140, 357, 573, 580). The mean resident flora of the hands of surgeons was reduced by a 3-min application of 4% chlorhexidine from 3.5 log10 units (preoperatively) to 3.15 log10 units (postoperatively) in operations lasting less than 2 h. It has been shown that for operations lasting more than 3 h, 4% chlorhexidine was unable to keep the resident skin bacteria below the baseline value (4.5 preoperatively and 5.2 postoperatively) (76).

(iv) Resistance.

The definition of chlorhexidine resistance is often based on a report from 1982 in which the MICs of chlorhexidine for 317 clinical isolates of P. aeruginosa were analyzed, leading to the suggestion that resistance to chlorhexidine should be reported if the MIC is ≥50 mg/liter (390).

Resistance to chlorhexidine among gram-positive bacterial species is rather uncommon. Among Streptococcus and Enterococcus species, no chlorhexidine resistance has been demonstrated (42, 231). However, gram-negative bacteria, such as E. coli (389), Proteus mirabilis (100, 536), Providencia stuartii (227, 228, 554), P. aeruginosa (390, 556), P. cepacia (348), and S. marcescens (291), have frequently been reported to be resistant to chlorhexidine. The frequency of resistance for the different species is variable. A total of 84.6% of clinical isolates of P. mirabilis must be considered resistant to chlorhexidine (536). Among other gram-negative bacteria, the rate is lower (42, 195). C. albicans was found to have a resistance rate of 10.5% (42, 231).

Acquired resistance to chlorhexidine has been reported to occur in S. aureus (249) and among many gram-negative bacteria (37, 38, 434) which were isolated after recurrent bladder washouts using 600 mg of chlorhexidine per liter (537, 538) or after addition of chlorhexidine to catheter bags for paraplegic patients (584). Some of the isolates were highly resistant, with chlorhexidine MICs of ≥500 mg/liter (538). The chlorhexidine resistance is quite clearly linked to hospital isolates only. A selection of 196 environmental gram-negative isolates did not reveal a resistance to chlorhexidine (147).

High chlorhexidine MICs correlate with poor reduction in the number of test bacteria in suspension tests, which highlights the potential hazard (555). The MIC may be as high as 1600 μg/ml and correlates well with a slow and insufficient bacterial reduction in suspension tests, as shown with strains of Providencia (539). The resistance may be single (83), but cross-resistance to other anti-infective agents can also occur. Among isolates of P. aeruginosa from industry and hospitals, an association between resistance to antibiotics and chlorhexidine has been described (290). The potential for cross-resistance between antiseptic agents and antibiotics must be given careful consideration (443). Various nonfermenting gram-negative bacteria which were isolated from blood cultures of oncology patients were inactivated only with >500 mg of chlorhexidine per liter (210).

Different mechanisms of resistance have been found. The acquired resistance is probably linked to the inner (227) or the outer (551) membrane of bacterial cells, the cell surface (131), or the cell wall (549). It may also be explained by the presence of plasmids which code for chlorhexidine resistance (269) and may therefore be transfered to other bacterial species (486, 619). A change in lipid content or a reduced adsorption of the antiseptic can be excluded as the main mechanism of resistance, as shown with isolates from urinary tract infections caused by P. mirabilis (554) and S. marcescens (410).

Recurrent exposure of bacteria to chlorhexidine may lead to adaptation and may enhance their resistance. This phenomenen was shown with S. marcescens. One example involves repeated exposure to various contact lens solutions containing between 0.001 and 0.006% chlorhexidine, which enabled S. marcescens to multiply in the disinfectant solution (154). Repeated exposure of P. aeruginosa to 5 mg of chlorhexidine per liter was shown to increase the MIC from <10 to 70 mg/liter within 6 days (556). A similar result was reported with Pseudomonas stutzeri, which became resistant (MIC, 50 mg/liter) after 12 days of exposure to chlorhexidine (550). Even with Streptococcus sanguis, a clear increase of the chlorhexidine MIC during permanent chlorhexidine exposure was observed (601). In general, higher exposures to chlorhexidine in hospitals were reported to be associated with higher rates of resistance (67). Recently, some isolates of P. aeruginosa. K. pneumoniae, and A. baumannii isolated from soap dispensers were reported to multiply in a 1:2 dilution of a 2% chlorhexidine liquid soap; ATCC strains of K. pneumoniae and A. baumannii multiplied only at higher dilutions (73). The latter report highlights the potential danger for the hospital.

Resistance to chlorhexidine may even result in nosocomial infections. Occasional outbreaks of NIs have been traced to contaminated solutions of chlorhexidine (345). There is one report that a 0.5% chlorhexidine solution which was used to disinfect plastic clamps for Hickman lines and was handled by health care workers who transmitted the adapted bacteria to intravenous lines led to 12 cases of bacteremia with three fatalities (357). In another outbreak, contamination of a disinfectant solution with Burkholderia multivorans led to nine cases of surgical site infection (45). Especially when chlorhexidine resistance is endemic in gram-negative bacteria, the use of chlorhexidine-based hand antiseptics may lead to an increase of NIs by the chlorhexidine-resistant species (100).

Effect on human skin.

Chlorhexidine gluconate is among the most common antiseptics causing ICD (540). However, the frequency of hand dermatitis associated with chlorhexidine-containing detergents is concentration dependent; products containing 4% chlorhexidine cause dermatitis much more frequently than do those containing lower concentrations (540). However, even preparations with the same concentration of chlorhexidine (4%) may cause skin irritation at different frequencies (398, 508). The differences are presumably due to other components of the various formulations. The relatively large number of reports of dermatitis related to chlorhexidine gluconate was partly explained by the fact that it was one of the most widely used antiseptics. In a survey of over 400 nurses working in several hospitals, detergents containing chlorhexidine were reported to cause skin damage less frequently than was nonantimicrobial soap or other detergents containing antimicrobial agents (298). In one 5-day prospective clinical trial, a detergent containing 4% chlorhexidine gluconate caused less irritation than did plain bar soap (300). Nonetheless, dry skin may occur with repeated exposure to preparations containing 4% chlorhexidine gluconate (339, 398).

The potential for contact allergy has been studied as well. Among eczema patients, 5.4% were found to have a positive skin reaction after a single patch test with 1% chlorhexidine, indicating the presence of an allergic contact dermatitis. Repeated exposure resulted in a sensitization rate of ca. 50% (310). In another study, 15 (2.5%) of 551 patients showed a strong and obviously relevant skin reaction in a single patch test with 1% chlorhexidine (415). Although these studies were carried out with patients and not with health care workers, the results nevertheless indicate the potential for sensitization and allergic contact dermatitis during frequent use. Allergic reactions to the use of detergents containing chlorhexidine gluconate on intact skin have been reported and can be severe, including dyspnea and anaphylactic shock (30, 92, 124, 138, 158, 270, 409, 425, 430, 468, 526, 563). Some cases of contact urticaria have also occurred as a result of chlorhexidine use (141, 617).

In summary, chlorhexidine (2 to 4%) has good activity against most vegetative bacteria, yeasts, and enveloped viruses but limited activity against mycobacteria, dermatophytes, and naked viruses. It has a moderate potential for acquired bacterial resistance. A hand wash with a chlorhexidine-based soap can reduce the number of transient bacteria by 2.1 to 3 log10 units; the effect on the resident hand flora is smaller, with a mean reduction between 0.35 and 2.29 log10 units. The dermal tolerance is rather poor, and anaphylactic reactions have been reported (Table 9).

Triclosan

Triclosan is one of many phenol derivatives (diphenoxyethyl ether) which have been used as a group of active agents since 1815, when coal tar was used for disinfection (222). Ever since, many different derivatives, such as thymol, cresol, and hexachlorophene, have been isolated and synthesized. Some of them have been used in antiseptic soaps for health care workers. Triclosan was introduced in 1965 and has been marketed as cloxifenol, Irgasan CH 3565, and Irgasan DP 300. It has very good stability (585) and resists diluted acid and alkali (453). The commonly used concentration in antiseptic soaps is 1%.

The mode of action of triclosan was identified some years ago. For decades, it has been assumed that triclosan attacks the bacterial cytoplasmic membrane (372, 458). Since 1998, we have known that it blocks lipid synthesis by inhibition of the enzyme enoyl-acyl carrier protein reductase, which plays an essential role in lipid synthesis (367). Mutation and overexpression of the fabI gene—which encodes the enoyl-acyl carrier protein reductase—are able to abolish the blockage of lipid synthesis caused by triclosan (205, 312). The fabI gene was first found in E. coli (366) and was subsequently also found in various other bacterial species such as P. aeruginosa (215), S. aureus (203, 520), and M. smegmatis (365). Some other bacteria, such as Bacillus subtilis, contain orthologous enoyl-acyl carrier protein reductases, namely those encoded by fabI and fabK, which are not inhibited by triclosan (204, 206). A genetic sequence coding for broad-spectrum resistance to triclosan has been identified (239).

The identification of the specific mode of action has raised concerns about the development of resistance to triclosan (313, 366, 506). A recent study has shown that this concern is valid. Strains of P. aeruginosa were exposed to triclosan and subsequently developed multiresistance to various antibiotics, including ciprofloxacin (86). Particular care should be taken in the use of triclosan in ICUs, where P. aeruginosa is the most common nosocomial pathogen, causing lower respiratory tract infection (260).

Effect on microorganisms and viruses. (i) Spectrum of activity.

In vitro, triclosan exhibits a bacteriostatic effect at lower concentrations (575); at higher concentrations, it has bactericidal activity (560). The activity of triclosan is greater against gram-positive organisms than against gram-negative bacteria, particularly P. aeruginosa (238). MIC of triclosan generally range between 0.025 and 4 mg/liter among isolates of S. aureus and MRSA (94, 459, 543). The fungicidal activity of triclosan is good and includes yeasts and dermatophytes (459).

(ii) Testing under practical conditions.

For artificially contaminated hands, a 1-min hand wash with 0.1% triclosan has been shown to reduce the number of test bacteria by 2.8 log10 units (475), which is essentially identical to the results obtained with nonmedicated soap (257). A soap based on 1% triclosan was found to reduce the resident hand flora within 5 min by 0.6 log10 unit (305). A 2% concentration yielded no major difference at 0.8 log10 unit (49). If hands were contaminated with rotavirus and treated with 2% triclosan for 30 s, the number of test viruses was reduced by 2.1 log10 units (47). On the resident hand flora, 1 or 2% triclosan has only a small effect, showing a mean reduction between 0.29 and 0.8 log10 unit within 5 min (Table 8).

(iii) In-use tests.

In comparison to plain soap, at 0.2% triclosan does not further reduce bacterial counts on the hands (295). Under clinical conditions, a hand wash with 1% triclosan was reported to be less effective on the total bacterial count than a 4% chlorhexidine hand wash (140). Triclosan was able to eliminate MRSA from the hands (140). In contrast, gram-negative bacteria were less likely to be eliminated after the use of triclosan (140).

(iv) Resistance.

One S. aureus isolate for which the triclosan MIC is >6,400 mg/liter has been described (494). Some isolates of gram-negative bacteria have been found with triclosan MICs of >100 mg/liter as well (459). This high resistance was not transferable and was probably chromosomal (494). Exposure of S. aureus to 0.01% triclosan over 28 days did not result in a change of the triclosan MIC (543). Using S. epidermidis in a similar test, however, resulted in an increase of the MIC from 2.5 to 20 mg/liter, indicating a high potential for adaptation of the bacterium (545). Exposure of P. aeruginosa to 25 mg of triclosan per liter yielded multiresistant mutants which exhibited resistance to triclosan (MIC, >128 mg/liter) and some antibiotics, e.g., tetracycline (MIC, >256 mg/liter), trimethoprim (MIC, >1,024 mg/liter), and erythromycin (MIC, >1,024 mg/liter) (86).

An antiseptic hand wash preparation based on 1% triclosan was found to be contaminated with S. marcescens in an operating theater and a surgical ICU (43). This involved 4 (17%) of 23 bottles and 5 (28%) of 18 wall dispensers, but no association with a higher rate of NIs was found (43).

The widespread use of triclosan in antibacterial household products such as liquid soaps is cause for concern that selection for bacteria with an intrinsic resistance to triclosan may be occurring (314). Triclosan can be found in 76% of antibacterial liquid soaps in the United States (424), which has led to the recommendation that it should not be used in consumer products (547). It is therefore not surprising that highly resistant bacteria were detected in compost, water, and soil (369). Two species, Pseudomonas putida and Alcaligenes xylosoxidans, were even capable of metabolizing triclosan and thereby of actively “digesting” the active agent (369).

Effect on human skin.

Detergents containing less than 2% triclosan are generally well tolerated. In one laboratory-based study of surgical hand disinfectants, a detergent containing 1% triclosan caused fewer subjective skin problems than did formulations containing an iodophor, 70% ethanol plus 0.5% chlorhexidine gluconate, or 4% chlorhexidine gluconate (305). Allergic reactions to triclosan-based handwash products are uncommon (616).

In summary, triclosan (1 to 2%) has good activity against vegetative bacteria and yeasts but limited activity against mycobacteria and dermatophytes. The activity against viruses is unknown. Triclosan has a low potential for acquired bacterial resistance. A hand wash with a triclosan-based soap can reduce the number of transient bacteria by 2.8 log10 units; the effect on the resident hand flora is lower, yielding a mean reduction between 0.29 and 0.8 log10 unit. The dermal tolerance is rather poor (Table 9).

Ethanol, Isopropanol, and n-Propanol

The general antimicrobial activity of alcohols has been described to increase with the length of the carbon chain and reaches a maximum at six carbon atoms (548). Solubility in water has led to a preference for ethanol and the two propanols. Alcohols have a nonspecific mode of action, consisting mainly of denaturation and coagulation of proteins (241). Cells are lysed (229, 428), and the cellular metabolism is disrupted (360).

Ethanol is a well-known antimicrobial agent, which was first recommended for the treatment of hands in 1888 (473). The antimicrobial activity of isopropanol (equivalent to propan-2-ol) and n-propanol (equivalent to propan-1-ol) was first investigated in 1904 (612). Many studies followed and supported the use of the two propanols for hand disinfection (52, 85, 322, 395).

Both the alkyl chain length and branching affect the antimicrobial activity (562). The following ranking regarding the bactericidal activity has been generally established: n-propanol > isopropanol > ethanol (95, 476, 548). The bactericidal activity is also higher at 30 to 40°C than at 20 to 30°C (561). In terms of virucidal activity, ethanol is superior to the propanols.

Effect on microorganisms and viruses. (i) Spectrum of activity.

(a) Ethanol. Ethanol has a strong immediate bactericidal activity (297) that is observed at 30% and higher concentrations (383, 444, 448, 449). Against S. aureus. E. faecium, or P. aeruginosa, its bactericidal activity seems to be slightly higher, at 80% than at 95% (110). According to the tentative final monograph for health care antiseptic products, ethanol is considered to be generally effective at between 60 and 95% (21). The spectrum of bactericidal activity of ethanol is broad (198).

Ethanol is also effective against various mycobacteria. Ethanol at 95% killed M. tuberculosis in sputum within 15 s, 70% ethanol required a contact time of 30 s, and 50% ethanol required 60 s (524), which was also required against M. smegmatis (54). Similar results were obtained with 70% ethanol and M. tuberculosis (55). For Mycobacterium terrae, the surrogate test strain for M. tuberculosis, a log10 reduction of >4 was found with 85% ethanol within 30 s (258). Very good activity was also shown with 70% ethanol against M. bovis (56).

In addition, ethanol has broad activity against most fungi—including yeasts and dermatophytes—at different exposure times and under different test conditions (56, 134, 258, 285, 286, 331).

The spectrum of virucidal activity is largely dependent on the concentration of ethanol. Higher concentrations of ethanol (e.g., 95%) generally have better virucidal activity than do lower concentrations, such as 60 to 80%, especially against naked viruses (127, 244, 534). A hand rub based on 95% ethanol has been described to have broad virucidal activity within 2 min, even against the most common nonenveloped viruses such as poliovirus and adenovirus (19). A gel based on 85% ethanol was still effective with a reduction factor (RF) of >4 against poliovirus within 3 min and against adenovirus within 2 min (258). Most naked viruses such as poliovirus (258, 262, 268, 535, 566), astroviruses (288), feline calicivirus (164), rotaviruses (258, 288), and echoviruses (287, 288) are inactivated by ethanol as well. HAV may be the only virus which is not fully inactivated; however, a higher RF of 3.2 was found with 95% ethanol whereas the RF was only 1.8 with 80% ethanol (615). Preparations containing less than 85% ethanol are usually less effective against viruses (570), although they may reveal sufficient activity within 10 min against various nonenveloped viruses such as adenovirus, poliovirus, echovirus, or Coxsackie virus (268). Under variable test conditions and at different exposure times, ethanol has broad general activity against the enveloped viruses, such as vaccinia virus (61, 184, 185, 268), influenza A virus (185, 268), togaviruses (77), Newcastle disease virus (97), HIV (346, 529), HBV (68, 272), and herpes simplex viruses (268).

Ethanol is known to have virtually no sporicidal activity (56, 165). This was first described over a century ago (135, 199, 395, 461). A pseudo-outbreak was reported due to contamination of ethanol with spores of B. cereus. The ethanol was used in the hospital pharmacy for preparation of skin antiseptics without spore filtration (219). Another report described contamination of 70% ethanol with spores of Clostridium perfringens, which was eliminated by addition of 0.27% hydrogen peroxide over 24 h (602).

(b) Isopropanol. The bactericidal activity of isopropanol begins at a concentration of 30% (445) and increases with increasing concentration but is lower again at 90% (544). It is similar to the bactericidal activity of n-propanol (612). In suspension tests, a hand rub based on propanols (total of 75%, wt/wt) had a comprehensive bactericidal activity against 13 gram-positive species, 18 gram-negative species, and 14 emerging pathogens within 30 s. Test bacteria included both ATCC strains and clinical isolates (248). Variations of the test conditions (e.g., with organic load) usually have no effect on the overall result in suspension tests (253). A tuberculocidal activity was found with isopropanol between 50 and 70% (150). The virucidal activity against naked viruses is limited and usually does not include enteroviruses such as astrovirus or echovirus (287, 288). If the exposure time is extended, sufficient activity against some nonenveloped viruses—such as echovirus (90% isopropanol for 10 min), feline calicivirus (50 to 70% isopropanol for ≥3 min), or adenovirus (50% isopropanol for 10 min)—can be achieved (164, 268). Isopropanol alone has no sporicidal activity, as shown with spores of B. subtilis and Clostridium novyi (445).

(c) n-Propanol. As early as 1904, n-propanol was described as an alcohol with a very strong bactericidal effect (548, 612) starting at a concentration of 30% (250). Compared to isopropanol, the activity against feline calicivirus seems to be better (164). In general, however, the antimicrobial activity of n-propanol is thought to be similar to that of isopropanol (475).

(ii) Testing under practical conditions.

(a) Ethanol. On hands artificially contaminated with E. coli, ethanol at concentrations between 70 and 80% caused a reduction in the number of test organisms of between 3.8 and 4.5 log10 units within 60 s (475-477), and 1.96 log10 units within 10 s (23). Significant differences may be observed among alcohol-based gels. Up to an ethanol concentration of 70%, gels have been described to be significantly less effective than the reference hand disinfection (282, 432). A preparation with 85% ethanol, however, was found to be as effective as the reference hand disinfection, with 3 ml within 30 s (258).

Other types of artificial contamination of hands have only rarely been tested. Using S. aureus, a 30-s application of 70% ethanol achieved a 2.6 or 3.7 log10 unit reduction (34, 318). A similar result was found with 79% ethanol against Micrococcus luteus (mean RF, 3.2 after 30 s) (174). If hands were contaminated with rotavirus and treated with 70% ethanol for 10 s, the number of test virus was reduced by 2.05 log10 units (23). A longer application time of 30 s revealed a similar reduction of 2.72 log10 units (47). Low ethanol concentrations, e.g., 70 or 62%, did not even achieve a 1 log10-unit reduction of HAV on contaminated hands (355) but achieved a 2.9 to 4.2 log10-unit reduction within 20 s against adenovirus, rhinovirus, and rotavirus (496). Contamination with poliovirus was reduced by only 1.6 log10 units within 10 s by use of 70% ethanol (534). A solution of 80% ethanol reduced the carriage of poliovirus on fingers by only 0.4 log10 unit within 30 s (106). A higher concentration of ethanol (95%) reduced different naked viruses, such as adenovirus (RF, >2.3), poliovirus (RF, between 0.7 and 2.5), and coxsackievirus (RF, 2.9), significantly better on the hands (504). Against feline calicivirus, a sufficient efficacy (RF ≥ 3.83) was observed with 70% ethanol within 1 min without an organic load (164). Experiments with 5% fecal test suspension as the organic load, however, demonstrated a lowered efficacy of ethanol. Within 30 s, ethanol at 70% revealed a mean log10 reduction between 1.27 and 1.56 (244) and ethanol at 95% was more effective (mean RF between 1.63 and 2.17) (244).

The lack of sporicidal efficacy has been recently confirmed under practical conditions of hand contamination, using spores of B. atrophaeus, a surrogate for B. anthracis (594).

The effect on the resident hand flora depends on the ethanol concentration and the application time. A reduction between 1.0 and 1.5 log10 units has been found with ethanol at 70 and 80% within 2 min; higher concentrations (80 and 85%) and longer application times led to mean reductions between 2.1 and 2.5 log10 units (Table 8).

Comparison to antimicrobial soaps or nonmedicated soaps usually reveals the superior efficacy of ethanol on the resident hand flora or on artificial contamination of hands with E. coli or S. marcescens (32, 34, 66, 80, 267, 318, 377, 406, 419, 476). To date, there is only one study with a 2-min application time, yielding the opposite result (319). Other test models have been investigated as well. Compared to washing hands with plain soap, a 30-s hand disinfection using 70% ethanol was significantly more effective in reducing the transfer of Staphyloccocus saprophyticus (344). The higher bactericidal efficacy of ethanol than of antimicrobial soaps is even more pronounced in the presence of blood (296, 297).

Comparison to other alcohols reveals only minor differences. Using S. marcescens as a test organism, 70% ethanol with 0.5% chlorhexidine was described to be more effective under practical conditions than was 70% isopropanol, which may be explained by the different type of alcohol, the additional chlorhexidine, or both (14).

(b) Isopropanol. Isopropanol (60%) has been chosen as the reference agent for testing the efficacy of hygienic hand disinfection in European standard EN 1500 (116). With the reference treatment on hands which were artificially contaminated with E. coli and treated with two 3-ml doses for a total of 60 s, a mean reduction of 4.6 log10 units was achieved (256, 257). In other studies, similar results of 4.0 to 4.4 log10 units within 60 s were found (472, 475, 480, 482). The reduction with 70% isopropanol after 10 s, however, is 2.15 log10 units (23). In contrast, a gel based on 60% isopropanol was found to be significantly less effective than three liquid rinses against three test bacteria at 15 and 30 s (110). Using bacteria other than E. coli to artificially contaminate hands, similar mean reductions were found after 30 s in S. aureus (mean RF, 6.36), E. faecalis (mean RF, 6.07), and P. aeruginosa (mean RF, 6.81) (110). After 15 s, mean RFs were only marginally lower in S. aureus (mean RF, 5.90), E. faecalis (mean RF, 5.03), and P. aeruginosa (mean RF, 6.05) (110). If hands were contaminated with rotavirus and treated with 70% isopropanol for 10 s, the number of test viruses was reduced by 99.8% (RF, 2.7). The number of E. coli cells is reduced to a similar extent (99%; RF, 2.0) (23). A similar result was obtained when hands were contaminated with rotavirus and treated with 70% isopropanol for 30 s. The number of test viruses was reduced by 3.1 log10 units (47). Contamination with poliovirus was reduced only by 0.8 log10 units within 10 s after use of 70% isopropanol (534). The efficacy against feline calicivirus is also quite low, with a mean reduction of 0.76 log10 unit (90% isopropanol) or 2.15 log10 units (70% isopropanol) within 30 s (164).

Isopropanol at 60 and 70% has a rather low efficacy against the resident hand flora within 2 min (RF, between 0.7 and 1.2). With longer application times (3 and 5 min) and higher concentrations of isopropanol (80 and 90%), the mean reduction of the resident hand flora is between 1.5 and 2.4 (Table 8).

Comparison of isopropanol with nonmedicated soaps and antimicrobial soaps reveals the better efficacy of isopropanol, both on the resident hand flora (129, 316) and on hands which were artificially contaminated (33, 44, 472), with only one study showing discrepant results (306).

(c) n-Propanol. On hands which were artificially contaminated with E. coli, n-propanol at 100, 60, or 50% reduced the number of test bacteria within 1 min by 5.8, 5.5, or 5.0 log10 units, respectively (482, 604). Lower concentrations, e.g., 40%, still reduce the test bacteria by 4.3 log10 unit within 1 min (475). The efficacy against feline calicivirus seems to be quite good, with a mean RF between 1.9 (80% n-propanol) and ≥ 4.13 (50% n-propanol) within 30 s (164). Against the resident hand flora, 60% n-propanol is quite effective, with a mean reduction of 1.1 after 1 min and of 2.05 to 2.9 after 5 min (Table 8). A combination of isopropanol (45%) with n-propanol (30%) is significantly more efficacious than n-propanol (60%) on the resident hand flora in two studies; yielding a mean RF of 4.61 versus 2.9 in one study (240) and a mean RF of 1.45 versus 0.83 in the other (341).

(iii) In-use tests.

(a) Ethanol. During an outbreak of gentamicin-resistant Klebsiella aerogenes, a health care worker was found to carry the strain on her hand. K. aerogenes was still detectable on two occasions after use of 95% ethanol for hand disinfection. The nurse continued to carry the strain for almost 4 weeks on her hand (82). Especially among health care workers wearing artificial fingernails, ethanol (60%) was found to be more effective in the removal of nosocomial pathogens than was an antimicrobial soap (368).

(b) Isopropanol. Under clinical conditions, a combination of isopropanol, n-propanol, and mecetronium etilsulfate was found to be significantly more effective than a chlorhexidine-based liquid soap (168). Isopropanol at 60% was found to have a better bactericidal efficacy on the resident hand flora than do antiseptic soaps based on chlorhexidine or triclosan (382). The higher bactericidal efficacy of isopropanol compared to antimicrobial soaps is even more pronounced in the presence of blood (296, 297).

Isopropanol at 60 to 70% was found to be necessary for removal of aerobic gram-negative bacteria from hands, whereas a simple hand wash with soap was inadequate (125). Transmission of gram-negative bacteria was also significantly better interrupted by propanol than by a social hand wash following brief contact with a heavily contaminated patient source (129).

(c) n-Propanol. Comparisons of n-propanol with nonmedicated soaps and antimicrobial soaps consistently reveal the greater efficacy of n-propanol on hands which were artificially contaminated (33, 480, 482). Comparison between n-propanol and isopropanol reveals a slightly greater efficacy of n-propanol (33). The efficacy of 60% n-propanol was found to be similar to that of 90% isopropanol on the resident bacteria (483).

(iv) Resistance.

No acquired resistance to ethanol, isopropanol, or n-propanol has been reported to date.

Effect on human skin.

Alcohols are considered to be among the safest antiseptics available and generally have no toxic effect on human skin (332). One of the first studies was carried out in 1923 and found that isopropanol had no noticeable harmful effect on human skin (181). This has been confirmed in a repetitive occlusive patch test with n-propanol at various concentrations (333). In addition, different formulations based on various alcohols were tested on intact skin for 6 days and 4 weeks and were well tolerated (279). The skin barrier remains intact, dermal hydration does not change significantly, and the dermal sebum content remains unchanged (279). A similar result was found in a repetitive occlusive patch test with an ethanol-based hand gel (255) and a propanol-based hand rub (254). Even on preirritated skin, the potential for irritation by commonly used alcohols is very low (333). Repeated exposure to alcohol or a moderately formulated product can cause or maintain skin dryness and irritation (108, 197, 475). Ethanol is less cytotoxic (278) and may be less irritating than n-propanol or isopropanol (108, 281, 423). Adding 1 to 3% glycerol, humectants, emollients, or other skin-conditioning agents can reduce or eliminate the drying effects of alcohol (34, 182, 306, 328, 396, 408, 481, 587).

Various studies have addressed the question whether alcohol-based hand rubs have a dermal tolerance that is similar to or better than that of nonmedicated or antimicrobial soaps. Several prospective trials have demonstrated that alcohol-based hand rubs containing emollients may cause significantly less skin dryness and irritation than washing hands with liquid detergents (70, 303, 304, 378, 611). For example, a prospective, randomized clinical trial with crossover design was conducted with nurses working on several hospital wards in order to compare hand washing with a nonantimicrobial liquid detergent and hand disinfection using a commercially available alcohol hand gel. The condition of the skin of nurses' hands was determined at the beginning, midpoint, and end of each phase of the trial by using participants' self-assessment, visual assessment by an observer, and objective assessment of skin dryness via measurements of the electrical capacitance of the skin on the dorsal surface of the hands. Self-assessments and visual assessments by the observer both found that skin irritation and dryness occurred significantly less often when nurses routinely used the alcohol-based hand gel between attending to patients, and electrical skin capacitance readings demonstrated that skin dryness occurred significantly less often when the alcohol hand gel was used (70). A questionnaire study conducted at the end of the trial found that more than 85% of nurses felt that the alcohol hand rub caused less skin dryness than did washing with soap and water and that they would be willing to use the product routinely for hand hygiene (69). In another study of 77 operating-room staff who used either an alcohol-based hand rub or an antiseptic liquid soap for surgical hand disinfection, skin dryness and skin irritation decreased significantly in the group using the alcohol rub whereas they both increased in the group using soap (416). In another clinical trial, nurses were randomly assigned to use either a nonantimicrobial liquid detergent or an alcohol-based hand rinse, and skin tolerance was studied by using a combination of self-assessments, evaluations by a dermatologist, and measurements of TEWL. Self-assessments and those of the dermatologist found that the alcohol hand rinse was tolerated significantly better than the liquid detergent (611). There was no significant difference in TEWL readings with the two regimens. In a prospective, randomized trial conducted with ICU personnel, the effects on skin condition of a detergent containing 2% chlorhexidine were compared to those of an alcohol-based hand rub. Both the skin scaling scores and self-assessments found that the alcohol-based hand rub was tolerated better than the detergent containing 2% chlorhexidine (303). In a similar randomized, prospective trial in a neonatal ICU, the alcohol-based hand rinse regimen was tolerated significantly better than a detergent containing 2% chlorhexidine (301).

In a prospective intervention trial designed to study the impact of introducing an alcohol hand rinse on hand hygiene compliance among health care workers, dermatologist-assessed skin dryness and irritation revealed that the alcohol hand rinse was tolerated better than the traditional antiseptic hand-washing preparation (167). Measurements of skin hydration improved (although not significantly) after the alcohol hand rinse was introduced. Other clinical studies have also shown that alcohol-based hand rubs are tolerated well by health care workers (351). Furthermore, in a laboratory-based study of hand disinfection which compiled observations by an expert, self-assessments, and TEWL measurements, an alcohol-based hand rub caused less skin irritation than did a detergent containing 2% chlorhexidine (186).

Another trial based only on self-assessments to determine the impact on skin condition of an alcohol hand rub versus a detergent containing 4% chlorhexidine gluconate also found that the alcohol-based product was better tolerated (384).

In health care facilities where hand washing with plain soap or antimicrobial soap and water has been the rule, switching (particularly in the winter) to an alcohol-based hand rub may cause some personnel to complain of burning or stinging of the skin when applying alcohol. This is usually due to the presence of underlying, detergent-associated ICD among personnel (252). Skin that has been damaged by preexisting exposure to detergents may be more susceptible to irritation by alcohols than are nondamaged skin areas (333). As the skin condition improves with continued use of alcohol-based hand rubs, the burning and stinging associated with applying alcohol invariably disappears.

Allergic contact dermatitis or contact urticaria syndrome induced by exposure to alcohol-based hand rubs occurs rarely (88), and the cause is not clear. For example, surveillance at a large hospital where a commercial alcohol hand rub has been used for more than 10 years has not identified a single case of well-documented allergy to the product (606). In the few observed cases, however, it remains unclear whether the allergic reaction to the product is caused by the ethanol or by any of the auxiliary agents of the formulation (88). When reactions do occur, they may be caused by hypersensitivity to the alcohol itself, to aldehyde metabolites, or to some other additive (413). Allergic reactions to ethanol or isopropanol have been reported, are extremely rare (413), and depend on the chemical purity of the tested alcohol. Other ingredients in alcohol-based hand rubs that could be responsible for allergic reactions include fragrances, stearyl or isostearyl alcohol, benzyl alcohol, myristyl alcohol, phenoxyethanol, propylene glycol, parabens, and benzalkonium chloride (28, 107, 152, 189, 413, 442, 620).

In summary, ethanol (60 to 85%), isopropanol (60 to 80%) and n-propanol (60 to 80%) have very good activity against vegetative bacteria, mycobacteria, yeasts, dermatophytes, and enveloped viruses. Ethanol is more effective against naked viruses than are isopropanol and n-propanol. None of the alcohols has a potential for acquired bacterial resistance. Hand disinfection with an alcohol-based hand rub can reduce transient bacteria by 2.6 to 6.8 log10 units, but the effect on the resident hand flora is lower, with a mean reduction between 1.5 and 2.9 log10 units. The dermal tolerance is good (Table 9).

EFFECT ON NOSOCOMIAL INFECTIONS

Plain Soap (Social Hand Wash)

Compared with no hand washing at all, a simple hand wash reduces the transmission of nosocomial pathogens. Enforcement of a simple hand wash together with other infection control measures on a neonatal ICU led to a significant reduction of rectal colonization with VRE among newborns (40.2 versus 7%) (340). The simple hand wash has also been shown to be effective after direct contact with contaminated objects and before meals for prevention of infectious enteritis caused by Salmonella enterica servar Enteritidis (149). A similar effect on the incidence of diarrhea has been reported from India, although the hand wash had no effect on diarrhea caused by rotaviruses (512). One study exists which shows an effect even on the transmission of respiratory tract viruses. More frequent hand washing by health care workers in combination with cohorting of patients with respiratory tract infections caused by RSV has been found to reduce the nosocomial spread of RSV (225). Although these studies indicate that hand washing can reduce the transmission of nosocomial pathogens, especially during outbreak investigations involving multiple control measures, it is impossible to determine the individual contribution made by hand hygiene in preventing transmission.

Overall, wet hands have been described to significantly increase the risk of cross-transmission, indicating that hands should always be thoroughly dried (373).

Chlorhexidine and Triclosan (Hygienic Hand Wash)

Only a few studies were available which examined the impact of antimicrobial soaps on NIs. One study looked at the colonization and infection rate with Klebsiella spp. in an ICU. The annual rate was reduced from 22% in 1972 and 22.6% in 1973 to 15.5% in 1974, which was explained mainly by the introduction of a chlorhexidine-based liquid soap (81). In another study, NIs were less frequent when personnel performed antiseptic hand washing instead a simple hand wash (339). Antiseptic hand washing was also associated with lower NI rates in some ICUs but not in others (349). Some investigators have found that nosocomial acquisition of MRSA was reduced when the antimicrobial soap used for hand washing was changed (597, 621).

Ethanol, Isopropanol, and n-Propanol

The use of alcohol-based hand rubs in regular patient care and its promotion over the years resulted in an increase of compliance in hand hygiene from 48 to 66% and a decreased in the rate of NIs from 16.9 to 9.9% at the same time. This is a significant decrease, of 41.1% in the NI rate (439). A comparative study of ICUs was carried out to determine the efficacy of a chlorhexidine-based soap (4%) and an isopropanol-based hand rub (60%) with the optional use of bland soap in reducing NIs. Washing hands with the chlorhexidine-based soap resulted in a lower rate of NIs, but the difference was not significant. However, it has been stated that this study does not indicate which of the two hand hygiene treatments is superior in ICUs. The personnel used much smaller volumes of isopropanol than of chlorhexidine and washed their hands more often than they used the hand rub (117). The data should therefore be regarded as resulting from a comparison between a social hand wash and chlorhexidine rather than a comparison between isopropanol and chlorhexidine (170). On a single ward in a 498-bed acute-care facility, use of an alcohol-based hand preparation over a 10-month period resulted in a 36% decrease in the incidence of two indicator NIs (urinary tract infections and surgical-site infections), expressed as the infection rate per 1,000 patient-days (211). In another study with an ethanol-based hand gel, the incidence of C. difficile-associated diarrhea decreased from 11.5 to 9.5 cases per 1,000 admissions within 1 year, but the difference was not significant (172). At the same time, the incidence of hospital-acquired MRSA decreased from 50 to 39% (172). Introduction of an ethanol-based hand disinfectant in a neonatal ICU significantly reduced cross-transmission of K. pneumoniae within 3 months from 21.5 to 4.7 cases of nosocomial colonization per 1,000 patient-days (75). Cross-transmission of E. faecium and C. albicans decreased as well, while rates for E. coli. Enterobacter agglomerans, and E. faecalis remained low and almost unchanged (75). The use of a virucidal hand rub based on 95% ethanol was part of an effective outbreak management of gastroenteritis caused by norovirus which involved 63 patients and health care workers (263).

EFFECT ON COMPLIANCE WITH HAND HYGIENE PRACTICES

Compliance with hand hygiene practices is known to be low. Compliance rates have been described to vary between 16 and 81% (437), with an overall average of 40% (71). One of the main goals of the new CDC guideline on hand hygiene is to provide evidence-based recommendations for improvement of compliance with hand hygiene (71). It is known that strategies to improve compliance with hand hygiene practices should be multimodal and multidisciplinary (435). Many individual parameters with a proven effect on hand hygiene compliance, however, have been identified in the new CDC guideline (71). These are efficacy, dermal tolerance, accessibility, time required for the procedure education, and personal perception; they are discussed below.

Hospital personnel should be provided with efficacious hand hygiene products, such as alcohol-based hand rubs. A change of the hand hygiene agent has been described to be particularly beneficial in institutions or hospital wards with a high workload and a high demand for hand hygiene (71).

Hand-washing agents are known to cause irritation and dryness, resulting in lower compliance rates (71). Hand hygiene products should have a low irritancy potential, particularly when these products are used multiple times per shift. A change to alcohol-based hand rubs should be made with great care, especially during winter, when hand skin is more irritable (252). Provision of skin care products may help (71, 437). However, they should not impair the efficacy of agents applied to the hands (71).

Easy access to a fast-acting hand hygiene agents should be viewed as the main tool of the strategy (71, 435, 437). Hand hygiene should be made possible, easy, and convenient. In areas with high workload, alcohol-based hand rubs should be made available at the entrance to the patient's room or at the bedside, in other convenient locations, or in individual pocket-sized bottles to be carried by health care workers (71).

Insufficient time to carry out the procedure, e.g., caused by high workload or understaffing, is associated with poor compliance (71). The time required for nurses to leave a patient's bedside, to to a sink, and wash and dry their hands before attending the next patient is a deterrent to a high compliance rate (71). A hand wash may take 62 s, whereas only one-fourth that time is required to use an alcohol-based hand rub placed at the bedside (579).

Ongoing education and promotion of hand hygiene should accompany the introduction of alcohol-based hand rubs in order to achieve long-lasting improvement in hand hygiene practices. Educational elements should include topics such as the rationale for hand hygiene, indications for hand hygiene, techniques of hand hygiene, methods to maintain hand skin health, and the correct use of gloves (71).

The smell, consistency (“feel”), and color may be important characteristics of the hand hygiene preparation that can influence the compliance rate by affecting the personal perception of those who use it (71). Differences in the acceptability of various agents have been described (258, 279, 349).

As well as the above parameters, the choice of the agent and the contents of a preparation may well have an impact on the compliance rate (242, 349, 481). The choice of a hand hygiene agent has been described to be one of many factors contributing to a strategy to successfully promote hand hygiene in hospitals (436). Baseline compliance rates in different departments vary between 30 and 63% for any soap, including plain and medicated soap, and sometimes even with the optional use of alcohol-based hand rubs if no intervention is done (Table 10). Several other studies have been conducted to measure the effect of various interventions on compliance rates with hand hygiene practices. In many studies the agent for hand hygiene remained unchanged. A higher compliance rate could be achieved by educational and training. In other studies, introduction of an alcohol-based hand rub or gel was accompanied by an educational and motivational campaign. Compliance rates could also be increased, often to a higher rate compared with the rate associated with no change of the hand hygiene agent (Table 11). Introduction of ethanol-based hand rubs sometimes revealed lower compliance rates and sometimes revealed higher compliance rates, with a trend toward the higher rates. The acceptability of the preparation and the role model function of physicians apparently have considerable influence. Preparations based on isopropanol or a combination of isopropanol and n-propanol revealed consistently higher compliance rates if education and promotion are carried out during introduction of the preparation and if the preparation has a superior dermal tolerance (Table 11). A 25% increase of compliance with hand hygiene is possible (64) with the right choice of agent (which should have an excellent dermal tolerance and a high acceptability among users) and with an intensive educational and promotional campaign. These data very much support the recommendation of the CDC guideline to choose hand hygiene products with a low irritance potential and with a maximum acceptability by health care workers (71). The acceptability includes an assessment of the feel, fragrance, and subjective skin tolerance of the product (71). In this respect, well-formulated preparations based on propanol have been shown to have a better acceptability in terms of skin tolerance and skin dryness (279).

TABLE 10.

Baseline compliance rates in hand hygiene, according to the agent

Type of ward(s) Type of agent(s)a Baseline compliance rate (%) Reference(s)
Pediatric ICU Soap 30.1 118
All wards Soap 30.2 592
Long-term care Soap 31.9 558
All wards Soap 32 334
Pediatric ICU Soap 34 196
Medical ICU Soap 38.1 10
All wards Soap 45 293
Surgical ICU Soap 45 429
ICU and oncology ward Soap 56 515
Medical ICU Soap 60.7 266
ICU Soap 61.4 530
ICU Soap 63.1 261
Neonatal ICU and infant rehydration unit Plain soap 29 308
ICU Medicated soap (4% chlorhexidine) 42 117
ICU Plain soap and alcohol 38b 117
ICU Plain soap and alcohol 40.2 622
Emergency department Plain soap and isopropanol (60%) 32.3 370
All Plain soap and isopropanol (70%) 48 439
ICU Medicated soap (chlorhexidine) and alcohol 28.7 176
ICU Alcohol 55.2 126
a

“Soap” was always assumed to be meant when “hand washing” was mentioned in a study; it may include plain and medicated soap.

b

Low compliance was explained by incorrect and rare use of alcohol.

TABLE 11.

Compliance rates in hand hygiene, according to the agent and intervention

Type of ward(s) Agent(s)a (baseline) Main active agent(s)a (new) Intervention(s) Compliance rate (%)
Main reason(s) for change Reference
Baseline After intervention
ICU Soap Soap Lectures, feedback, demonstrations 5 63 Lectures, feedback, demonstrations 51
ICU Soap Soap New design of ICU 16 30 More convenient sink location 446
ICU Soap Soap Education 22.0 29.9 Education 518
ICU Soap Soap Lectures and reminder labels on ventilators 46 (before patient contact), 83 (after patient contact) 92 (before patient contact), 92 (after patient contact) Lectures and reminder labels on ventilators 264
Pediatric ambulatory setting Soap Soap Use of reminders 49 49 Use of reminders 324
Pediatric wards Soap Soap Educational program 52 74 Educational program 31
Emergency department Soap Soap Posting of signs, education 54 64 Posting of signs, education 120
Neonatal ICU Soap Soap Use of gowns 62 60 Use of gowns 421
ICU Soap Soap Performance feedback and new soap 63 92 Performance feedback 352
ICU Soap Soap Education and feedback 81 92 Education and feedback 122
Surgical ICU Plain and medicated soap (chlorhexidine) Plain and medicated soap (chlorhexidine) Automatic hand-washing machines available 22 38 Availability of hand-washing machines 618
New-burn nursersies Medicated soap Medicated soap Feedback 28 63 Feedback 451
Medical ICU Medicated soap Medicated soap Routine wearing of gowns and gloves, educational meetings 40.8 58.2 Routine wearing of gowns and gloves, educational meetings 521
ICU Medicated soap (para-chloro- metaxylenol) Medicated soap (para-chlorometaxylenol) Teaching and reminders (buttons) 22 29.9 Reminders 518
Medical ICU Medicated soap (4% chlorhexidine) Medicated soap (4% chlorhexidine) Education 26% (before patient contact), 23% (after patient contact) 38% (before patient contact), 60% (after patient contact) Education 91
Pediatric ICU Soap (plain and medicated), ethanol (70%), aqueous povidone iodine Soap (plain and medicated), ethanol (70%), aqueous povidone iodine Overt observation and feedback 12% (before patient contact), 11% (after patient contact) 68% (before patient contact), 65% (after patient contact) Overt observation and feedback 559
ICU Soap Ethanol (60%) Quality improvement and introduction of hand gel 42.5 35.1 “Sticky uncomfortable feeling” of product 197
ICU and medical ward Plain and medicated soap (4% chlorhexidine) Ethanol (60%) Education program followed by introduction of hand rub 16.3 20.9 (after education), 33.2 (after introduction of hand rub) Easy access of hand rub 63
Medical ICU and ward Soap Ethanol (62%) Introduction of hand rub with an educational and motivational campaign; wall dispensers Overall, 60%; medical ICU, 70.3%; ward, 46.2% Overall, 52%; Medical ICU, 58%; ward, 48% Physicians as role models 388
Plastic surgery department Soap Ethanol (70%) Performance feedback 62 61.3 Performance feedback 336
Neonatal ICU Plain soap Ethanol (79%) Introduction of hand rub and quality improvement 44 48 Unknown 75
ICU Soap Isopropanol (60%) Introduction of hand rub and teaching 32 45 Accessability of hand rub 180
ICU Plain soap Isopropanol (75%) Promotion campaign for hand hygiene 38.4 54.5 Campaign on benefits of alcohol-based hand rubs 223
All Isopropanol (75%) Promotion campaign for hand hygiene 48 66 Campaign on benefits of alcohol-based hand rubs 439
Medical ICU Plain soap Isopropanol (45%) and n-propanol (30%) Introduction of hand rub and education 42.2 60.9 Availability of hand rub; short time for hand rub procedure 351
All Soap (plain and medicated) Isopropanol (45%) and n-propanol (30%) Introduction of hand rub and education 62.2 66.5 Better dermal tolerance of hand rub 167
All Soap (plain and medicated) Isopropanol (45%) and n-propanol (30%) Introduction of hand rub and education 52 66 Dermal tolerance and accessibility 169
a

“Soap” was always assumed to be meant when “hand washing” was mentioned in a study; it may include plain and medicated soap.

CONCLUSION

The social hand wash has only a few indications in hospitals and community medicine (243): mechanical cleaning when hands are visibly soiled with blood or other body fluids, before eating and after using the restroom, and if contamination of hands with bacterial spores is suspected (71). In these clinical situations, the simple hand wash reveals the best results compared with other possible hand treatments.

In the CDC guideline, a hygienic hand disinfection with an alcohol-based hand rub is the preferred treatment to be carried out after patient care activities that could lead to contamination of the hands of the health care workers, e.g., after contact with the patient's intact skin, body fluids or excretions, mucous membranes, nonintact skin, and wound dressings (if hands are not visibly soiled), when moving from a contaminated body site to a clean body site, after contact with environmental surfaces in the immediate vicinity of patients, and after glove removal (71). Hands should also be treated before having direct contact with patients, before donning sterile gloves when inserting devices such as vascular lines, indwelling urinary catheters, or peripheral vascular catheters (71). Hand hygiene is also indicated after using the restroom in cases of diarrhea and after blowing the nose in cases of an upper respiratory tract infection (18). The use of antimicrobial soaps in all these situations will probably be less effective in preventing cross-transmission of nosocomial pathogens and also has the risk of inducing occupational ICD.

REFERENCES

  • 1.Abad, F. X., R. M. Pinto, and A. Bosch. 1994. Survival of enteric viruses on environmental fomites. Appli. Environ. Microbiol. 60:3704-3710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Abad, F. X., C. Villena, S. Guix, S. Caballero, R. M. Pintó, and A. Bosch. 2001. Potential role of fomites in the vesicular transmission of human astroviruses. Appl. Environ. Microbiol. 67:3904-3907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Abrishami, S. H., B. D. Tall, T. J. Bruursema, P. S. Epstein, and D. B. Shah. 1994. Bacterial adherence and viability on cutting board surfaces. J. Food Saf. 14:153-172. [Google Scholar]
  • 4.Adams, B. G., and T. J. Marrie. 1982. Hand carriage of aerobic Gram-negative rods by health care personnel. J. Hyg. (London) 89:23-31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Adams, B. G., and T. J. Marrie. 1982. Hand carriage of aerobic Gram-negative rods may not be transient. J. Hyg. (Cambridge) 89:33-45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Aho, L. S., I. Simon, J. B. Bour, L. Morales-Gineste, P. Pothier, and J. B. Gouyon. 2000. Epidemiology of viral nosocomial infections in pediatrics. Pathol. Biol. 48:885-892. [PubMed] [Google Scholar]
  • 7.Aiello, A. E., J. Cimiotti, P. Della-Latta, and E. L. Larson. 2003. A comparison of the bacteria found on the hands of “homemakers” and neonatal intensive care unit nurses. J. Hosp. Infect. 54:310-315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Aitken, C., and D. J. Jeffries. 2001. Nosocomial spread of viral disease. Clin. Microbiol. Rev. 14:528-546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Akhter, J., S. al-Hajjar, S. Myint, and S. M. Qadri. 1995. Viral contamination of environmental surfaces on a general paeditric ward and playroom in a major referral centre in Riyadh. Eur. J. Epidemiol. 11:587-590. [DOI] [PubMed] [Google Scholar]
  • 10.Albert, R. K., and F. Condie. 1981. Hand-washing patterns in medical intensive-care units. N. Engl. J. Med. 304:1465-1466. [DOI] [PubMed] [Google Scholar]
  • 11.Alfurayh, O., A. Sabeel, M. N. Al Ahdal, K. Almeshari, G. Kessie, M. Hamid, and D. M. Dela Cruz. 2000. Hand contamination with hepatitis C virus in staff looking after hepatitis C-positive hemodialysis patients. Am. J. Nephrol. 20:103-106. [DOI] [PubMed] [Google Scholar]
  • 12.Allaker, R. P., and W. C. Noble. 1993. Microbial interaction on skin, p. 331-354. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 13.Aly, R., and H. I. Maibach. 1979. Comparative study on the antimicrobial effect of 0.5% chlorhexidine gluconate and 70% isopropyl alcohol on the normal flora of hands. Appl. Environ. Microbiol. 37:610-613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Aly, R., and H. I. Maibach. 1980. A comparison of the antimicrobial effect of 0.5% chlorhexidine (Hibistat) and 70% isopropyl alcohol on hands contaminated with Serratia marcescens. Clin. Exp. Dermatol. 5:197-201. [DOI] [PubMed] [Google Scholar]
  • 15.Aly, R., and H. I. Maibach. 1981. Factors controlling skin bacterial flora, p. 29-39. In H. I. Maibach and R. Aly (ed.), Skin microbiology, relevance to clinical infection. Springer-Verlag, New York, N.Y.
  • 16.Anagnostakis, D., J. Fitsialos, C. Koutsia, J. Messaritakis, and N. Matsaniotis. 1981. A nursery outbreak of Serratia marcescens infection. Evidence of a single source of contamination. Am. J. Dis. Child. 135:413-414. [DOI] [PubMed] [Google Scholar]
  • 17.Anonymous. 2001. British Pharmacopoeia. The Stationary Office, London, United Kingdom.
  • 18.Anonymous. 2000. Händehygiene. Bundesgesundheitsblatt 43:230-233. [Google Scholar]
  • 19.Anonymous. 2003. Liste der vom Robert Koch-Institut geprüften und anerkannten Desinfektionsmittel und -verfahren. Bundesgesundheitsblatt 46:74-95. [DOI] [PubMed] [Google Scholar]
  • 20.Anonymous. 2002. National nosocomial infections surveillance (NNIS) system report, data summary from January 1992-June 2002. Am. J. Infec. Control 30:458-475. [DOI] [PubMed] [Google Scholar]
  • 21.Anonymous. 1994. Tentative final monograph for health care antiseptic products: proposed rule. Fed. Regist. 59:31401-31452. [Google Scholar]
  • 22.Ansari, S. A., S. A. Sattar, V. S. Springthorpe, G. A. Wells, and W. Tostawaryk. 1988. Rotavirus survival on human hands and transfer of infectious virus to inanimate and nonporous inanimate surfaces. J. Clin. Microbiol. 26:1513-1518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Ansari, S. A., S. A. Sattar, V. S. Springthorpe, G. A. Wells, and W. Tostowaryk. 1989. In vivo protocol for testing efficacy of hand-washing agents against viruses and bacteria: experiments with rotavirus and Escherichia coli. Appl. Environ. Microbiol. 55:3113-3118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Ansari, S. A., V. S. Springthorpe, and S. A. Sattar. 1991. Survival and vehicular spread of human rotaviruses: possible relation to seasonality of outbreaks. Rev. Infect. Dis. 13:448-461. [DOI] [PubMed] [Google Scholar]
  • 25.Ansari, S. A., V. S. Springthorpe, S. A. Sattar, S. Rivard, and M. Rahman. 1991. Potential role of hands in the spread of respiratory viral infections: studies with human parainfluenza virus 3 and rhinovirus 14. J. Clin. Microbiol. 29:2115-2119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Asensio, A., R. Canton, J. Vaque, J. Rossello, and J. L. Arribas. 2002. Etiology of hospital-acquired infections in Spanish hospitals (EPINE, 1990-1999). Med. Clin. 118:725-730. [DOI] [PubMed] [Google Scholar]
  • 27.Astagneau, P., C. Rioux, F. Golliot, and G. Brucker. 2001. Morbidity and mortality associated with surgical site infections: results from the 1997-1999 INCISO surveillance. J. Hosp. Infect. 48:267-274. [DOI] [PubMed] [Google Scholar]
  • 28.Aust, L. B., and H. Maibach. 1980. Incidence of human skin sensitization to isostearyl alcohol in two separate groups of panelists. Contact Dermatitis 6:269-271. [DOI] [PubMed] [Google Scholar]
  • 29.Austin, D. J., M. J. M. Bonten, R. A. Weinstein, S. Slaughter, and R. M. Anderson. 1999. Vancomycin-resistant enterococci in the intensive-care hospital settings: transmission dynamics, persistance, and the impact of infection control programs. Proc. Nat. Acad. Sci. USA 96:6908-6913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Autegarden, J.-E., C. Pecquet, S. Huet, O. Bayrou, and F. Leynadier. 1999. Anaphylactic shock after application of chlorhexidine to unbroken skin. Contact Dermatitis 40:215. [DOI] [PubMed] [Google Scholar]
  • 31.Avila-Agüero, M., M. A. Umanza, A. L. Jiménez, I. Faingezicht, and M. M. Paris. 1998. Handwashing practices in a tertiary-care, pediatric hospital and the effect on an educational program. Clin. Perform. Qual. Health Care 6:70-72. [PubMed] [Google Scholar]
  • 32.Ayliffe, G. A. J., J. R. Babb, K. Bridges, H. A. Lilly, E. J. L. Lowbury, J. Varney, and M. D. Wilkins. 1975. Comparison of two methods for assessing the removal of total organisms and pathogens from the skin. J. Hyg. (Cambridge) 75:259-274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Ayliffe, G. A. J., J. R. Babb, J. G. Davies, and H. A. Lilly. 1988. Hand disinfection: a comparison of various agents in laboratory and ward studies. J. Hosp. Infect. 11:226-243. [DOI] [PubMed] [Google Scholar]
  • 34.Ayliffe, G. A. J., J. R. Babb, and A. H. Quoraishi. 1978. A test for “hygienic” hand disinfection. J. Clin. Pathol. 31:923-928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Azar, M. J., D. K. Dhaliwal, K. S. Bower, R. P. Kowalski, and Y. J. Gordon. 1996. Possible consequences of shaking hands with your patients with epidemic keratoconjunctivitis. Am. J. Ophthalmol. 121:711-712. [DOI] [PubMed] [Google Scholar]
  • 36.Babb, J. R., J. G. Davies, and G. A. J. Ayliffe. 1991. A test procedure for evaluating surgical hand disinfection. J. Hosp. Infect. 18:41-49. [DOI] [PubMed] [Google Scholar]
  • 37.Baillie, L. 1987. Chlorhexidine resistance among bacteria isolated from urine of catheterized patients. J. Hosp. Infect. 10:83-86. [DOI] [PubMed] [Google Scholar]
  • 38.Baillie, L. 1986. Routine screening of catheter urine specimens for chlorhexidine resistant organisms. Med. Lab. Sci. 43:284-285. [PubMed] [Google Scholar]
  • 39.Bale, M. J., P. M. Bennett, J. E. Benninger, and M. Hinton. 1993. The survival of bacteria exposed to desiccation on surfaces associated with farm buildings. J. Appl. Bacteriol. 75:519-528. [DOI] [PubMed] [Google Scholar]
  • 40.Barbut, F., and J. C. Petit. 2001. Epidemiology of Clostridium difficile-associated infections. Clin. Microbiol. Infect. 7:405-410. [DOI] [PubMed] [Google Scholar]
  • 41.Bardell, D. 1989. Hand-to-hand transmission of herpes simplex virus type 1. Microbios 59:93-100. [PubMed] [Google Scholar]
  • 42.Barry, A. L., P. C. Fuchs, and S. D. Brown. 1999. Lack of effect of antibiotic resistance on susceptibility of microorganisms to chlorhexidine gluconate or povidone iodine. Eur. J. Clin. Microbiol. Infect. Dis. 18:920-921. [DOI] [PubMed] [Google Scholar]
  • 43.Barry, M. A., D. E. Craven, T. A. Goularte, and D. A. Lichtenberg. 1984. Serratia marcescens contamination of antiseptic soap containing triclosan: implications for nosocomial infections. Infect. Control 5:427-430. [DOI] [PubMed] [Google Scholar]
  • 44.Bartzokas, C. A., M. F. Gibson, R. Graham, and D. C. Pinder. 1983. A comparison of triclosan and chlorhexidine preparations with 60 per cent isopropyl alcohol for hygienic hand disinfection. J. Hosp. Infect. 4:245-255. [DOI] [PubMed] [Google Scholar]
  • 45.Bassett, D. C. J., K. J. Stokes, and W. R. G. Thomas. 1970. Wound infection with Pseudomonas multivorans—a waterborne contaminant of disinfectant solution. Lancet i:1188-1189. [DOI] [PubMed] [Google Scholar]
  • 46.Bean, B., B. M. Moore, B. Sterner, L. R. Peterson, D. N. Gerding, and H. H. Balfour. 1982. Survival of influenza viruses an environmental surfaces. J. Infect. Dis. 146:47-51. [DOI] [PubMed] [Google Scholar]
  • 47.Bellamy, K., R. Alcock, J. R. Babb, J. G. Davies, and G. A. Ayliffe. 1993. A test for the assessment of “hygienic” hand disinfection using rotavirus. J. Hosp. Infect. 24:201-210. [DOI] [PubMed] [Google Scholar]
  • 48.Beltrami, E. M., I. T. Williams, C. N. Shapiro, and M. E. Chamberland. 2000. Risk and management of blood-borne infections in health care workers. Clin. Microbiol. Rev. 13:385-407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Bendig, J. W. A. 1990. Surgical hand disinfection: Comparison of 4% chlorhexidine detergent solution and 2% triclosan detergent solution. J. Hosp. Infect. 15:143-148. [DOI] [PubMed] [Google Scholar]
  • 50.Berardesca, E., G. P. Vignoli, F. Distante, P. Brizzi, and G. Rabbiosi. 1995. Effects of water temperature on surfactant-induced skin irritation. Contact Dermatitis 32:83-87. [DOI] [PubMed] [Google Scholar]
  • 51.Berg, D. E., R. C. Hershow, C. A. Ramirez, and R. A. Weinstein. 1995. Control of nosocomial infections in an intensive care unit in Guatemala City. Clin. Infect. Dis. 21:588-593. [DOI] [PubMed] [Google Scholar]
  • 52.Bernhardt, G. 1922. Über Isopropanol als Mittel zur Händedesinfektion. Deutsche Med. Wochenschr. 48:68-69. [Google Scholar]
  • 53.Bertrand, X., P. Bailly, G. Blasco, P. Balvay, A. Boillot, and D. Talon. 2000. Large outbreak in a surgical intensive care unit of colonization and infection with Pseudomonas aeruginosa that overexpressed an active efflux pump. Clin. Infect. Dis. 31:E9-E14. [DOI] [PubMed] [Google Scholar]
  • 54.Best, M., S. A. Sattar, V. S. Springthorpe, and M. E. Kennedy. 1988. Comparative mycobactericidal efficacy of chemical disinfectants in suspension and carrier tests. Appl. Environ. Microbiol. 54:2856-2858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Best, M., S. A. Sattar, V. S. Springthorpe, and M. E. Kennedy. 1990. Efficacies of selected disinfectants against Mycobacterium tuberculosis. J. Clin. Microbiol. 28:2234-2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Best, M., V. S. Springthorpe, and S. A. Sattar. 1994. Feasibility of a combined carrier test for disinfectants: studies with a mixture of five types of microorganisms. Am. J. Infect. Control 22:152-162. [DOI] [PubMed] [Google Scholar]
  • 57.Bettin, K., C. Clabots, P. Mathie, K. Willard, and D. N. Gerding. 1994. Effectiveness of liquid soap vs. chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hand. Infect. Control Hosp. Epidemiol. 15:697-702. [DOI] [PubMed] [Google Scholar]
  • 58.Bhalla, A., N. J. Pultz, D. M. Gries, A. J. Ray, E. C. Eckstein, D. C. Aron, and C. J. Donskey. 2004. Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients. Infect. Control Hosp. Epidemiol. 25:164-167. [DOI] [PubMed] [Google Scholar]
  • 59.Bidawid, S., J. M. Farber, and S. A. Sattar. 2000. Contamination of foods by food handlers: experiments on hepatitis A virus transfer to food and its interruption. Appl. Environ. Microbiol. 66:2759-2763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Bidawid, S., N. Malik, O. Adegbunrin, S. A. Sattar, and J. M. Farber. 2004. Norovirus cross-contamination during food handling and interruption of virus transfer by hand antisepsis: experiments with feline calicivirus. J. Food Prot. 67:103-109. [DOI] [PubMed] [Google Scholar]
  • 61.Bingel, K. F., and C. Hermann. 1966. Die experimentelle Desinfektion des Vakzinevirus als Grundlage für die klinische Pockenimpfung. Med. Welt 2:76-82. [PubMed] [Google Scholar]
  • 62.Birch, B. R., B. S. Perera, W. A. Hyde, V. Ruehorn, L. A. Ganguli, J. M. Kramer, and P. C. B. Turnbull. 1981. Bacillus cereus cross-infection in a maternity-unit. J. Hosp. Infect. 2:349-354. [DOI] [PubMed] [Google Scholar]
  • 63.Bischoff, W. E., T. M. Reynolds, C. N. Sessler, M. B. Edmond, and R. P. Wenzel. 2000. Handwashing compliance by health care workers: the impact of introducing an accessible, alcohol-based hand antiseptic. Arch. Intern. Med. 160:1017-1021. [DOI] [PubMed] [Google Scholar]
  • 64.Bissett, L. 2002. Can alcohol hand rubs increase compliance with hand hygiene? Br. J. Nurs. 11:1074-1077. [DOI] [PubMed] [Google Scholar]
  • 65.Blaschke-Hellmessen, R., M. Kreuz, and M. Sprung. 1985. Umweltresistenz und natürliche Keimreservoire medizinisch bedeutsamer Sprosspilze. Z. Gesamte Hyg. 31:712-715. [PubMed] [Google Scholar]
  • 66.Blech, M.-F., P. Hartemann, and J.-L. Paquin. 1985. Activity of non antiseptic soaps and ethanol for hand disinfection. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 181:496-512. [PubMed] [Google Scholar]
  • 67.Block, C., and M. Furman. 2002. Association between intensity of chlorhexidine use and microorganisms of reduced susceptibility in a hospital environment. J. Hosp. Infect. 51:201-206. [DOI] [PubMed] [Google Scholar]
  • 68.Bond, W. X. V., M. S. Favero, and N. Petersen, J. 1983. Inactivation of hepatitis B virus by intermediate to high-level disinfectant chemicals. J. Clin. Microbiol. 18:535-538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Boyce, J. M. 2001. Antiseptic technology: access, affordability and acceptance. Emerg. Infect. Dis. 7:231-233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Boyce, J. M., S. Kelliher, and N. Vallande. 2000. Skin irritation and dryness associated with two hand-hygiene regimens: soap-and-water hand washing versus hand antisepsis with an alcoholic hand gel. Infect. Control Hosp. Epidemiol. 21:442-448. [DOI] [PubMed] [Google Scholar]
  • 71.Boyce, J. M., and D. Pittet. 2002. Guideline for hand hygiene in health-care settings. Recommendations of the healthcare infection control practices advisory committee and the HICPAC/SHEA/APIC/IDSA hand hygiene task force. Morb. Mortal. Wkly. Rep. 51:1-45. [Google Scholar]
  • 72.Brady, M. T., J. Evans, and J. Cuartas. 1990. Survival and disinfection of parainfluenza viruses on environmental surfaces. Am. J. Infect. Control 18:18-23. [DOI] [PubMed] [Google Scholar]
  • 73.Brooks, S. E., M. A. Walczak, R. Hameed, and P. Coonan. 2002. Chlorhexidine resistance in antibiotic-resistant bacteria isolated from the surfaces of dispensers of soap containing chlorhexidine. Infect. Control Hosp. Epidemiol. 23:692-695. [DOI] [PubMed] [Google Scholar]
  • 74.Brouwer, D. H., R. Kroese, and J. J. van Hemmen. 1999. Transfer of contaminants from surface to hands: experimental assessment of linearity of the exposure process, adherence to the skin, and area exposed during fixed pressure and repeated contact with surfaces contaminated with a powder. Appl. Occup. Environ. Hyg. 14:231-239. [DOI] [PubMed] [Google Scholar]
  • 75.Brown, S. M., A. V. Lubimova, N. M. Khrustalyeva, S. V. Shulaeva, I. Tekhova, L. P. Zueva, D. Goldmann, and E. J. O'Rourke. 2003. Use of an alcohol-based hand rub and quality improvement interventions to improve hand hygiene in a Russian neonatal intensive care unit. Infect. Control Hosp. Epidemiol. 24:172-179. [DOI] [PubMed] [Google Scholar]
  • 76.Bryce, E. A., D. Spence, and F. J. Roberts. 2001. An in-use evaluation of an alcohol-based pre-surgical hand disinfectant. Infect. Control Hosp. Epidemiol. 22:635-639. [DOI] [PubMed] [Google Scholar]
  • 77.Bucca, M. A. 1956. The effect of various chemical agents on eastern equine encephalomyelitis virus. J. Bacteriol. 71:491-492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Burdon, D. W., and J. L. Whitby. 1967. Contamination of hospital disinfectants with Pseudomonas species. Br. Med. J. 2:153-155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Burnie, J. P., F. C. Odds, W. Lee, C., and J. D. Williams. 1985. Outbreak of systemic Candida albicans in intensive care units caused by cross infection. Br. Med. J. 290:746-748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Cardoso, C. L., H. H. Pereira, J. C. Zequim, and M. Guilhermetti. 1999. Effectiveness of hand-cleansing agents for removing Acinetobacter baumannii strain from contaminated hands. Am. J. Infect. Control 27:327-331. [DOI] [PubMed] [Google Scholar]
  • 81.Casewell, M., and I. Phillips. 1977. Hands as route of transmission for Klebsiella species. Br. Med. J. 2:1315-1317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Casewell, M. W., M. Webster, M. T. Dalton, and I. Phillips. 1977. Gentamicin-resistant Klebsiella aerogenes in a urological ward. Lancet ii:444-446. [DOI] [PubMed] [Google Scholar]
  • 83.Chawner, J. A., and P. Gilbert. 1989. Interaction of the bisbiguanides chlorhexidine and alexidine with phospholipid vesicles: evidence for separate modes of action. J. Appl. Bacteriol. 66:253-258. [DOI] [PubMed] [Google Scholar]
  • 84.Chow, C., A. Y. K. Chow, R. H. Downie, and H. S. Buttar. 1978. Percutanous absorption of hexachlorophen in rats, guinea pigs and pigs. Toxicology 9:147-154. [DOI] [PubMed] [Google Scholar]
  • 85.Christiansen, J. 1918. Zur Theorie und Praxis der Alkoholdesinfektion. Z. Physiol. Chem. 102:275-305. [Google Scholar]
  • 86.Chuanchuen, R., K. Beinlich, T. T. Hoang, A. Becher, R. R. Karkhoff-Schweizer, and H. P. Schweizer. 2001. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multi-drug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD- OprJ. Antimicrob. Agents Chemother. 45:428-432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Ciarlone, A. E., L. P. Gangarosa, and B. C. Fong. 1976. Detection of p-choraniline in chlorhexidine solutions using thin-layer chromatography. J. Dent. Res. 55:918-919. [DOI] [PubMed] [Google Scholar]
  • 88.Cimiotti, J. P., E. S. Marmur, M. Nesin, P. Hamlin-Cook, and E. L. Larson. 2003. Adverse reactions associated with an alcohol-based hand antiseptic among nurses in a neonatal intensive care unit. Am. J. Infect. Control 31:43-48. [DOI] [PubMed] [Google Scholar]
  • 89.Clark, T. A., and R. A. Hajjeh. 2002. Recent trends in the epidemiology of invasive mycoses. Curr. Opin. Infect. Dis. 15:569-574. [DOI] [PubMed] [Google Scholar]
  • 90.Cohen, H. A., E. Kitai, I. Levy, and D. Ben-Amitai. 2002. Handwashing patterns in two dermatology clinics. Dermatology 205:358-361. [DOI] [PubMed] [Google Scholar]
  • 91.Conly, J. M., S. Hill, J. Ross, J. Lertzman, and T. J. Louie. 1989. Handwashing practices in an intensive care unit: the effects of an educational program and its relationship to infection rates. Am. J. Infect. Control 17:330-339. [DOI] [PubMed] [Google Scholar]
  • 92.Conraads, V. M., P. G. Jorens, D. G. Ebo, M. J. Claeys, J. M. Bosmans, and C. J. Vrints. 1998. Coronary artery spasm complicating anaphylaxis secondary to skin disinfectant. Chest 113:1417-1419. [DOI] [PubMed] [Google Scholar]
  • 93.Cookson, B. D., M. C. Bolton, and J. H. Platt. 1991. Chlorhexidine resistance in methicillin-resistant Staphylococcus aureus or just an elevated MIC? An in vitro and in vivo assessment. Antimicrob. Agents Chemother. 35:1997-2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Cookson, B. D., H. Farrelly, P. Stapleton, R. P. J. Garvey, and M. R. Price. 1991. Transferable resistance to triclosan in MRSA. Lancet 337:1548-1549. [DOI] [PubMed] [Google Scholar]
  • 95.Coulthard, C. E., and G. Sykes. 1936. The germicidal effect of alcohol. Pharm. J. 137:79-81. [Google Scholar]
  • 96.Crémieux, A., M. E. Reverdy, J. L. Pons, C. Savage, J. Chevalier, J. Fleurette, and M. Mossé. 1989. Standardized method for evaluation of hand disinfection by surgical scrub formulations. Appl. Environ. Microbiol. 55:2944-2948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Cunningham, C. H. 1948. The effect of certain chemical agents on the virus of Newcastle disease of chicken. Am. J. Vet. Res. 9:195-197. [Google Scholar]
  • 98.Curley, A., R. E. Hawk, R. D. Kimbrough, G. Natheson, and L. Finberg. 1971. Dermal absorption of hexachlorophen in infants. Lancet ii:296-297. [DOI] [PubMed] [Google Scholar]
  • 99.D'Alessio, D. J., J. A. Peterson, C. R. Dick, and E. C. Dick. 1976. Transmission of experimental rhinovirus colds in volunteer married couples. J. Infect. Dis. 133:28-36. [DOI] [PubMed] [Google Scholar]
  • 100.Dance, D. A. B., A. D. Pearson, D. V. Seal, and J. A. Lowes. 1987. A hospital outbreak caused by a chlorhexidine- and antibiotic-resistant Proteus mirabilis. J. Hosp. Infect. 10:10-16. [DOI] [PubMed] [Google Scholar]
  • 101.Daschner, F. D. 1985. The transmission of infections in hospitals by staff carriers, methods of prevention and control. Infect. Control 6:97-99. [DOI] [PubMed] [Google Scholar]
  • 102.Dave, J., S. Reith, J. Q. Nash, R. R. Marples, and C. Dulake. 1994. A double outbreak of exfoliative toxin-producing strains of Staphylococcus aureus in a maternity unit. Epidemiol. Infect. 112:103-114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 103.Davies, D. J. G. 1978. Agents as preservatives in eye-drops and contact lense solutions. J. Appl. Bacteriol. 44:Sxix-Sxxviii. [DOI] [PubMed] [Google Scholar]
  • 104.Davies, G. E., J. Francis, A. R. Martin, F. L. Rose, and G. Swain. 1954. 1:6-Di-4′-chlorophenyldiguanidohexane (“Hibitane”*). Laboratory investigation of a new antibacterial agent of high potency. Br. J. Pharmacol. 9:192-196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 105.Davies, G. L., and J. Y. N. Lau. 1995. Hepatitis C, p. 2082-2114. In W. S. Haubrich, F. Schaffner, and J. E. Berk (ed.), Gastroenterology, 5th ed. The W. B. Saunders Co., Philadelphia, Pa.
  • 106.Davies, J. G., J. R. Babb, C. R. Bradley, and G. A. J. Ayliffe. 1993. Preliminary study of test methods to assess the virucidal activity of skin disinfectants using poliovirus and bacteriophages. J. Hosp. Infect. 25:125-131. [DOI] [PubMed] [Google Scholar]
  • 107.de Groot, A. C. 1987. Contact allergy to cosmetics: causative ingredients. Contact Dermatitis 17:26-34. [DOI] [PubMed] [Google Scholar]
  • 108.de Haan, P., H. H. M. Meester, and D. P. Brynzeel. 1996. Irritancy of alcohols, p. 65-70. In P. G. M. van der Valk and H. I. Maibach (ed.), The irritant contact dermatitis syndrome. CRC Press, Inc., Boca Raton, Fla.
  • 109.Demmler, G. J., M. D. Yow, S. A. Spector, S. G. Reis, M. T. Brady, D. C. Anderson, and L. H. Taber. 1987. Nosocomial cytomegalovirus infections within two hospitals caring for infants and children. J. Infect. Dis. 156:9-16. [DOI] [PubMed] [Google Scholar]
  • 110.Dharan, S., S. Hugonnet, H. Sax, and D. Pittet. 2003. Comparison of waterless hand antisepsis agents at short application times: raising the flag of concern. Infect. Control Hosp. Epidemiol. 24:160-164. [DOI] [PubMed] [Google Scholar]
  • 111.Dickgiesser, N. 1978. Untersuchungen über das Verhalten grampositiver und gramnegativer Bakterien in trockenem und feuchtem Milieu. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 167:48-62. [PubMed] [Google Scholar]
  • 112.Diekema, D. J., S. A. Messer, R. J. Hollis, R. P. Wenzel, and M. A. Pfaller. 1997. An outbreak of Candida parapsilosis prosthetic valve endocarditis. Diagn. Microbiol. Infect. Dis. 29:147-153. [DOI] [PubMed] [Google Scholar]
  • 113.Diekema, D. J., M. A. Pfaller, F.-J. Schmitz, J. Smayevsky, J. Bell, R. N. Jones, and M. Beach. 2001. Survey of infections due to Staphylococcus species: frequency of occurence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europa, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin. Infect. Dis. 32:S114-S132. [DOI] [PubMed] [Google Scholar]
  • 114.Dietze, B., A. Rath, C. Wendt, and H. Martiny. 2001. Survival of MRSA on sterile goods packaging. J. Hosp. Infect. 49:255-261. [DOI] [PubMed] [Google Scholar]
  • 115.DIN EN 1499. 1997. Chemische Desinfektionsmittel und Antiseptika. Desinfizierende Händewaschung. Prüfverfahren und Anforderungen (Phase 2/Stufe 2). Benth-Verlag, Berlin, Germany.
  • 116.DIN EN 1500. 1997. Chemische Desinfektionsmittel und Antiseptika. Hygienische Händedesinfektion. Prüfverfahren und Anforderungen (Phase 2/Stufe 2). Benth-Verlag, Berlin, Germany.
  • 117.Doebbeling, B. N., G. L. Stanley, C. T. Sheetz, M. A. Pfaller, A. K. Houston, L. Annis, N. Li, and R. P. Wenzel. 1992. Comparative efficacy of alternative hand-washing agents in reducing nosocomial infections in intensive care units. N. Engl. J. Med. 327:88-93. [DOI] [PubMed] [Google Scholar]
  • 118.Donowitz, L. G. 1987. Handwashing technique in a pediatric intensive care unit. Am. J. Dis. Child. 141:683-685. [DOI] [PubMed] [Google Scholar]
  • 119.Doring, G., S. Jansen, H. Noll, H. Grupp, F. Frank, K. Botzenhart, K. Magdorf, and U. Wahn. 1996. Distribution and transmission of Pseudomonas aeruginosa and Burkholderia cepacia in a hospital ward. Pediatr. Pulmonol. 21:90-100. [DOI] [PubMed] [Google Scholar]
  • 120.Dorsey, S. T., R. K. Cydulka, and C. L. Emerman. 1996. Is handwashing teachable? Failure to improve handwashing behavior in an urban emergency department. Acad. Emerg. Med. 3:360-365. [DOI] [PubMed] [Google Scholar]
  • 121.Drankiewicz, D., and L. Dundes. 2003. Handwashing among female college students. Am. J. Infect. Control 31:67-71. [DOI] [PubMed] [Google Scholar]
  • 122.Dubbert, P. M., J. Dolce, W. Richter, M. Miller, and S. W. Chapman. 1990. Increasing ICU staff handwashing: effects of education and group feedback. Infect. Control Hosp. Epidemiol. 11:191-193. [DOI] [PubMed] [Google Scholar]
  • 123.Dumpis, U., Z. Kovalova, J. Jansons, L. Cupane, I. Sominskaya, M. Michailova, P. Karayiannis, D. Gardovska, S. Viazov, S. Ross, M. Roggendorf, and P. Pumpens. 2003. An outbreak of HBV and HCV infection in a paediatric oncology ward: epidemiological investigation and prevention of further spread. J. Med. Virol. 69:331-338. [DOI] [PubMed] [Google Scholar]
  • 124.Ebo, D. G., W. J. Stevens, C. H. Bridts, and L. Matthieu. 1998. Contact allergic dermatitis and life-threatening anaphylaxis to chlorhexidine. J. Allergy Clin. Immunol. 101:128-129. [DOI] [PubMed] [Google Scholar]
  • 125.Eckert, R. N., N. J. Ehrenkranz, and B. C. Alfonso. 1989. Indications for alcohol or bland soap removal of of aerobic skin bacteria: assessment by a novel method. Infect. Control Hosp. Epidemiol. 10:306-311. [DOI] [PubMed] [Google Scholar]
  • 126.Eckmanns, T., A. Rath, H. Bräuer, F. Daschner, H. Rüden, and P. Gastmeier. 2001. Compliance der Händedesinfektion auf Intensivstationen. Dtsch. Med. Wochenschr. 126:745-749. [DOI] [PubMed] [Google Scholar]
  • 127.Eggers, H. J. 1990. Experiments on antiviral activity of hand disinfectants. Some theoretical and practical considerations. Zentbl. Bakteriol. 273:36-51. [DOI] [PubMed] [Google Scholar]
  • 128.Eggimann, P., J. Garbino, and D. Pittet. 2003. Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect. Dis. 3:685-702. [DOI] [PubMed] [Google Scholar]
  • 129.Ehrenkranz, N. J., and B. C. Alfonso. 1991. Failure of bland soap handwash to prevent hand transfer of patient bacteria to urethral catheters. Infect. Control Hosp. Epidemiol. 12:654-662. [DOI] [PubMed] [Google Scholar]
  • 130.Ekizoglu, M. T., M. Özalp, N. Sultan, and D. Gür. 2003. An investigation of the bactericidal effect of certain antiseptics and disinfectants on some hospital isolates of gram-negative bacteria. Infect. Control Hosp. Epidemiol. 24:225-227. [DOI] [PubMed] [Google Scholar]
  • 131.el Moug, T., D. T. Rogers, J. R. Furr, B. M. A. el Falaha, and A. D. Russell. 1985. Antiseptic-induced changes in the cell surface of a chlorhexidine-sensitive and a chlorhexidine-resistant strain of Providencia stuartii. J. Antimicrob. Chemother. 16:685-689. [DOI] [PubMed] [Google Scholar]
  • 132.El Shafie, S. S., M. Alishaq, and M. Leni Garcia. 2004. Investigation of an outbreak of multidrug-resistant Acinetobacter baumannii in trauma intensive care unit. J. Hosp. Infect. 56:101-105. [DOI] [PubMed] [Google Scholar]
  • 133.Emilson, A., M. Lindbert, and B. Forslind. 1993. The temperature effect of in vitro penetration of sodium lauryl sulfate and nickel chloride through human skin. Acta Dermatol. Venereol. 73:203-207. [DOI] [PubMed] [Google Scholar]
  • 134.Emmons, C. X. V. 1933. Fungicidal action of some common disinfectants on two dermatophytes. Arch. Dermatol. 28:15-21. [Google Scholar]
  • 135.Epstein, F. 1896. Zur Frage der Alkoholdesinfektion. Z. Hyg. 24:1-21. [Google Scholar]
  • 136.Esahli, H., K. Breback, R. Bennet, A. Ehrnst, M. Eriksson, and K. O. Hedlund. 1991. Astroviruses as a cause of nosocomial outbreaks of infant diarrhea. Pediatr. Infect. Dis. J. 10:511-515. [DOI] [PubMed] [Google Scholar]
  • 137.Evans, C. A., W. M. Smith, E. A. Johnston, and E. R. Giblett. 1950. Bacterial flora of the normal human skin. J. Investig. Dermatol. 15:305-324. [DOI] [PubMed] [Google Scholar]
  • 138.Evans, R. J. 1992. Acute anaphylaxis due to topical chlorhexidine acetate. Br. Med. J. 304:686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 139.Faix, R. G. 1987. Comparative efficacy of handwashing agents against cytomegalovirus. Infect. Control 8:158-162. [DOI] [PubMed] [Google Scholar]
  • 140.Faoagali, J. L., N. George, J. Fong, J. Davy, and M. Dowser. 1999. Comparison of the antibacterial efficacy of 4% chlorhexidine gluconate and 1% triclosan handwash products in an acute clinical ward. Am. J. Infect. Control 27:320-326. [DOI] [PubMed] [Google Scholar]
  • 141.Fisher, A. A. 1989. Contact urticaria from chlorhexidine. Cutis 43:17-18. [PubMed] [Google Scholar]
  • 142.Fitzgerald, K. A., A. Davies, and A. D. Russell. 1992. Effect of chlorhexidine and phenoxyethanol on cell surface hydrophobicity of Gram-positive and Gram-negative bacteria. Lett. Appl. Microbiol. 14:91-95. [Google Scholar]
  • 143.Flournoy, D. J., H. G. Muchmore, and E. B. Francis. 1979. Nosocomial infection linked to handwashing. Hospitals 53:105-107. [PubMed] [Google Scholar]
  • 144.Foca, M., K. Jakob, S. Whittier, P. Della Latta, S. Factor, D. Rubenstein, and L. Saiman. 2000. Endemic Pseudomonas aeruginosa infection in a neonatal intensive care unit. N. Engl. J. Med. 343:695-700. [DOI] [PubMed] [Google Scholar]
  • 145.Fox, M. K., S. B. Langner, and R. W. Wells. 1974. How good are hand washing practices. Am. J. Nurs. 74:1676-1678. [PubMed] [Google Scholar]
  • 146.Foxman, B. 2002. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am. J. Med. 113:5S-13S. [DOI] [PubMed] [Google Scholar]
  • 147.Freney, J., M. O. Husson, F. Gavini, S. Madier, A. Martra, D. Izard, H. Leclerc, and J. Fleurette. 1988. Susceptibilities to antibiotics and antiseptics of new species of the family Enterobacteriaceae. Antimicrob. Agents Chemother. 32:873-876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 148.Fridkin, S. K., and R. P. Gaynes. 1999. Antimicrobial resistance in intensive care units. Clin. Chest Med. 20:303-316. [DOI] [PubMed] [Google Scholar]
  • 149.Friedman, C. R., C. Torigian, P. J. Shillam, R. E. Hoffman, D. Heltzel, J. L. Beebe, G. Malcolm, W. E. DeWitt, L. Hutwagner, and P. M. Griffin. 1998. An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. J. Pediatr. 132:802-807. [DOI] [PubMed] [Google Scholar]
  • 150.Frobisher, M. 1953. A study of the effect of alcohols on tubercle bacilli and other bacteria in sputum. Am. Rev. Tuberc. 68:419-424. [DOI] [PubMed] [Google Scholar]
  • 151.Fryklund, B., K. Tullus, and L. G. Burman. 1995. Survival on skin and surfaces of epidemic and non-epidemic strains of enterobacteria from neonatal special care units. J. Hosp. Infect. 29:201-208. [DOI] [PubMed] [Google Scholar]
  • 152.Funk, J. O., and H. I. Maibach. 1994. Propylene glycol dermatitis: re-evaluation of an old problem. Contact Dermatitis 31:236-241. [DOI] [PubMed] [Google Scholar]
  • 153.Furuhashi, M., and T. Miyamae. 1979. Effect of pre-operative hand scrubbing and influence of pinholes appearing in surgical rubber gloves during operation. Bull. Tokyo Med. Dent. Univ. 26:73-80. [PubMed] [Google Scholar]
  • 154.Gandhi, P. A., A. D. Sawant, L. A. Wilson, and D. G. Ahearn. 1993. Adaption and growth of Serratia marcescens in contact lens disinfectant solutions containing chlorhexidine gluconate. Appl. Environ. Microbiol. 59:183-188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 155.Ganeswire, R., K. L. Thong, and S. D. Puthucheary. 2003. Nosocomial outbreak of Enterobacter gergoviae bacteraemia in a neonatal intensive care unit. J. Hosp. Infect. 53:292-296. [DOI] [PubMed] [Google Scholar]
  • 156.Garcia-Lechuz, J. M., S. Hernangomez, R. S. Juan, T. Pelaez, L. Alcala, and E. Bouza. 2001. Extra-intestinal infections caused by Clostridium difficile. Clin. Microbiol. Infect. 7:453-457. [DOI] [PubMed] [Google Scholar]
  • 157.Garcia-Martin, M., P. Lardelli-Claret, J. J. Jiménez-Moleón, A. Bueno-Cavanillas, J. D. Luna-del-Castillo, and R. Gálvez-Vargas. 2001. Proportion of hospital deaths potentially attributable to nosocomial infections. Infect. Control Hosp. Epidemiol. 22:708-714. [DOI] [PubMed] [Google Scholar]
  • 158.Garvey, L. H., J. Roed-Petersen, and B. Husum. 2001. Anaphylactic reactions in anaesthetised patients—four cases of chlorhexidine allergy. Acta Anaesthesiol. Scand. 45:1290-1294. [DOI] [PubMed] [Google Scholar]
  • 159.Gastmeier, P., G. Kampf, N. Wischnewski, T. Hauer, G. Schulgen, M. Schumacher, F. Daschner, and H. Rüden. 1998. Prevalence of nosocomial infections in representative German hospitals. J. Hosp. Infect. 38:37-49. [DOI] [PubMed] [Google Scholar]
  • 160.Gastmeier, P., G. Kampf, N. Wischnewski, M. Schumacher, F. Daschner, and H. Rüden. 1998. Importance of the surveillance method: national prevalence studies on nosocomial infections and the limits of comparison. Infect. Control Hosp. Epidemiol. 19:661-667. [DOI] [PubMed] [Google Scholar]
  • 161.Gastmeier, P., D. Sohr, C. Geffers, A. Nassauer, M. Dettenkofer, and H. Rüden. 2002. Occurrence of methicillin-resistant Staphylococcus aureus infections in German intensive care units. Infection 30:198-202. [DOI] [PubMed] [Google Scholar]
  • 162.Gaynes, R. P., D. H. Culver, T. C. Horan, J. R. Edwards, C. Richards, and J. S. Tolson. 2001. Surgical site infection (SSI) rates in the United States, 1992-1998: the national nosocomial infections surveillance system basic SSI risk index. Clin. Infect. Dis. 33:S69-S77. [DOI] [PubMed] [Google Scholar]
  • 163.Geffers, C., I. Zuschneid, D. Sohr, H. Rüden, and P. Gastmeier. 2004. Microbiological isolates associated with nosocomial infections in intensive care units: data of 274 intensive care units participating in the German nosocomial infections surveillance system (KISS). Anästhesiol. Intensivmed. Notfallmed. Schmerzther. 39:15-19. [DOI] [PubMed] [Google Scholar]
  • 164.Gehrke, C., J. Steinmann, and P. Goroncy-Bermes. 2004. Inactivation of feline calicivirus, a surrogate of norovirus (formerly Norwalk-like viruses), by different types of alcohol in vitro and in vivo. J. Hosp. Infect. 56:49-55. [DOI] [PubMed] [Google Scholar]
  • 165.Gershenfeld, L. 1938. The sterility of alcohol. Am. J. Med. Sci. 195:358-361. [Google Scholar]
  • 166.Getchell-White, S. I., L. G. Donowitz, and D. H. Groschel. 1989. The inanimate environment of an intensive care unit as a potential source of nosocomial bacteria: evidence for long survival of Acinetobacter calcoaceticus. Infect. Control Hos. Epidemiol. 10:402-407. [DOI] [PubMed] [Google Scholar]
  • 167.Girard, R., K. Amazian, and J. Fabry. 2001. Better compliance and better tolerance in relation to a well-conducted introduction to rub-in hand disinfection. J. Hosp. Infect. 47:131-137. [DOI] [PubMed] [Google Scholar]
  • 168.Girou, E., S. Loyeau, P. Legrand, F. Oppein, and C. Brun-Buisson. 2002. Efficacy of handrubbing with alcohol based solution versus standard handwashing with antiseptic soap: randomized clinical trial. Br. Med. J. 325:362-366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 169.Girou, E., and F. Oppein. 2001. Handwashing compliance in a French university hospital: new perspective with the introduction of hand-rubbing with a waterless alcohol-based solution. J. Hosp. Infect. 48:S55-S57. [DOI] [PubMed] [Google Scholar]
  • 170.Goldmann, D., and E. Larson. 1992. Hand-washing and nosocomial infections. N. Engl. J. Med. 327:120-122. [DOI] [PubMed] [Google Scholar]
  • 171.Goodall, R. R., J. Goldmann, and J. Woods. 1968. Stability of chlorhexidine solutions. Pharm. J. 200:33-34. [Google Scholar]
  • 172.Gopal Rao, G., A. Jeanes, M. Osman, C. Aylott, and J. Green. 2002. Marketing hand hygiene in hospitals—a case study. J. Hosp. Infect. 50:42-47. [DOI] [PubMed] [Google Scholar]
  • 173.Gorham, P., M. Millar, and P. G. R. Godwin. 1988. Clostridial hand-carriage and neonatal necrotising enterocolitis. J. Hosp. Infect. 12:139-141. [DOI] [PubMed] [Google Scholar]
  • 174.Goroncy-Bermes, P. 2001. Hand disinfection according to the European standard EN 1500 (hygienic hand rub): a study with Gram-negative and Gram-positive test organisms. Int. J. Hyg. Environ. Health 204:123-126. [DOI] [PubMed] [Google Scholar]
  • 175.Goroncy-Bermes, P., M. A. Schouten, and A. Voss. 2001. In vitro activity of a nonmedicated handwash product, chlorhexidine, and an alcohol-based hand disinfectant against multiply resistant gram-positive microorganisms. Infect. Control Hosp. Epidemiol. 22:194-196. [DOI] [PubMed] [Google Scholar]
  • 176.Gould, D. 1994. Nurses' hand decontamination practice: results of a local study. J. Hosp. Infect. 28:15-30. [DOI] [PubMed] [Google Scholar]
  • 177.Gould, D., and A. Chamberlain. 1997. The use of a ward-based educational teaching package to enhance nurses' compliance with infection control procedures. J. Clin. Nurs. 6:55-67. [DOI] [PubMed] [Google Scholar]
  • 178.Gould, J. C. 1963. Pseudomonas pyocyanea infections in hospitals, p. 119-130. In R. E. O. Williams and R. A. Shoother (ed.), Infection in hospitals. Blackwell Scientific Publications Ltd., Oxford, United Kingdom.
  • 179.Gräf; W., and W. Mönius. 1977. Staphylokokkenübertragung von Nase auf Hand und Brille, ein Hospitalismusproblem. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 164:127-137. [PubMed] [Google Scholar]
  • 180.Graham, M. 1990. Frequency and duration of handwashing in an intensive care unit. Am. J. Infect. Control 18:77-80. [DOI] [PubMed] [Google Scholar]
  • 181.Grant, D. H. 1923. Antiseptic and bactericidal properties of isopropylalcohol. Am. J. Med. Sci. 166:261-265. [Google Scholar]
  • 182.Gravens, D. L., H. R. Butcher, W. F. Ballinger, and N. E. Dewar. 1973. Septisol antiseptic foam for hands of operating room personnel: an effective antibacterial agent. Surgery 73:360-367. [PubMed] [Google Scholar]
  • 183.Grohskopf, L. A., V. R. Roth, D. R. Feikin, M. J. Arduino, L. A. Carson, J. I. Tokars, S. C. Holt, B. J. Jensen, R. E. Hoffman, and W. R. Jarvis. 2001. Serratia liquefaciens bloodstream infections from contamination of epoetin alfa at a hemodialysis center. N. Engl. J. Med. 344:1491-1497. [DOI] [PubMed] [Google Scholar]
  • 184.Grossgebauer, K. 1967. Zur Desinfektion der mit Pocken kontaminierten Hand. Gesundheitswes. Desinfekt. 59:1-12. [Google Scholar]
  • 185.Groupe, V., C. C. Engle, and P. E. Gaffney. 1955. Virucidal activity of representative anti-infective agents against influenza A and vaccinia virus. Appl. Microbiol. 3:333-336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 186.Grove, G. L., C. R. Zerweck, J. M. Heilman, and J. D. Pyrek. 2001. Methods for evaluating changes in skin condition due to the effects of antimicrobial hand cleaners: two studies comparing a new waterless chlorhexidine gluconate/ ethanol-emollient antiseptic preparation with a conventional water-applied product. Am. J. Infect. Control 29:361-369. [DOI] [PubMed] [Google Scholar]
  • 187.Guenthner, S. H., J. O. Hendley, and R. P. Wenzel. 1987. Gram-negative bacilli as nontransient flora on the hands of hospital personnel. J. Clin. Microbiol. 25:488-490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 188.Guilhermetti, M., S. E. Hernandes, Y. Fukushigue, L. B. Garcia, and C. L. Cardoso. 2001. Effectiveness of hand-cleansing agents for removing methicillin-resistant Staphylococcus aureus from contaminated hands. Infect. Control Hosp. Epidemiol. 22:105-108. [DOI] [PubMed] [Google Scholar]
  • 189.Guin, J. D., and J. Goodman. 2001. Contact urticaria from benzyl alcohol presenting as intolerance to saline soaks. Contact Dermatitis 45:182-183. [DOI] [PubMed] [Google Scholar]
  • 190.Gundermann, K.-O. 1972. Untersuchungen zur Lebensdauer von Bakterienstämmen im Staub unter dem Einfluß unterschiedlicher Luftfeuchtigkeit. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 156:422-429. [PubMed] [Google Scholar]
  • 191.Gwaltney, J. M., P. B. Moskalski, and J. O. Hendley. 1978. Hand-to-hand transmission of rhinovirus colds. Ann. Intern. Med. 88:463-467. [DOI] [PubMed] [Google Scholar]
  • 192.Haley, C. E., M. Marling-Cason, J. W. Smith, J. P. Luby, and P. A. Mackowiak. 1985. Bactericidal activity of antiseptics against methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 21:991-992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 193.Haley, R. W., D. H. Culver, J. W. White, W. M. Morgan, T. G. Emori, P. Van Munn, and T. M. Hooton. 1985. The efficacy of infection surveillance and control programs in preventing nosocomial infections in US hospitals. Am. J. Epidemiol. 121:182-205. [DOI] [PubMed] [Google Scholar]
  • 194.Hall, C. B. 2000. Nosocomial respiratory syncytial virus infections: the “cold war” has not ended. Clinic. Infect. Dis. 31:590-596. [DOI] [PubMed] [Google Scholar]
  • 195.Hammond, S. A., J. R. Morgan, and A. D. Russell. 1987. Comparative susceptibility of hospital isolates of gram-negative bacteria to antiseptics and disinfectants. J. Hosp. Infect. 9:255-264. [DOI] [PubMed] [Google Scholar]
  • 196.Harbarth, S., D. Pittet, L. Grady, and D. A. Goldmann. 2001. Compliance with hand hygiene practice in pediatric intensive care. Pediatr. Crit. Care Med. 2:311-314. [DOI] [PubMed] [Google Scholar]
  • 197.Harbarth, S., D. Pittet, L. Grady, A. Zawacki, G. Potter-Bynoe, M. H. Samore, and D. A. Goldmann. 2002. Interventional study to evaluate the impact of an alcohol-based hand gel in improving hand hygiene compliance. Pediatr. Infect. Dis. J. 21:489-495. [DOI] [PubMed] [Google Scholar]
  • 198.Hared, R., E. Baik, and S. Gash. 1963. Efficiency of antiseptics when acting on dried organisms. Br. Med. J. 1:496-500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 199.Harrington, C., and H. Walker. 1903. The germicidal action of alcohol. Boston Med. Surg. J. 148:548-552. [Google Scholar]
  • 200.Hassing, J. H., J. P. Nater, and E. Bleumink. 1982. Irritancy of low concentrations of soap and synthetic detergents as measured by skin water loss. Dermatologica 164:314-321. [DOI] [PubMed] [Google Scholar]
  • 201.Hay, R. J. 1993. Fungi and fungal infections of the skin, p. 232-263. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 202.Hayden, M. K. 2000. Insights into the epidemiology and control of infection with vancomycin-resistant enterococci. Clin. Infect. Dis. 31:1058-1065. [DOI] [PubMed] [Google Scholar]
  • 203.Heath, R. J., J. Li, G. E. Roland, and C. O. Rock. 2000. Inhibition of the Staphylococcus aureus NADPH-dependent enoyl-acyl carrier protein reductase by triclosan and hexachlorophene. J. Biol. Chem. 275:4654-4659. [DOI] [PubMed] [Google Scholar]
  • 204.Heath, R. J., and C. O. Rock. 2000. A triclosan-resistant bacterial enzyme. Nature 406:145-146. [DOI] [PubMed] [Google Scholar]
  • 205.Heath, R. J., J. R. Rubins, D. R. Holland, E. Zhang, M. E. Snow, and C. O. Rock. 1999. Mechanism if triclosan inhibition of bacterial fatty acid synthesis. J. Biol. Chem. 274:11110-11114. [DOI] [PubMed] [Google Scholar]
  • 206.Heath, R. J., N. Su, C. K. Murphy, and C. O. Rock. 2000. The enoyl-(acyl-carrier-protein) reductases FabI and FabL from Bacillus subtilis. J. Biol. Chem. 275:40128-40133. [DOI] [PubMed] [Google Scholar]
  • 207.Hedderwick, S. A., S. A. McNeil, M. J. Lyons, and C. A. Kauffman. 2000. Pathogenic organisms associated with artificial fingernails worn by health care workers. Infect. Control Hosp. Epidemiol. 21:505-509. [DOI] [PubMed] [Google Scholar]
  • 208.Heeg, P., W. Oβwald, and N. Schwenzer. 1986. Wirksamkeitsvergleich von Desinfektionsverfahren zur chirurgischen Händedesinfektion unter experimentellen und klinischen Bedingungen. Hyg. Med. 11:107-110. [Google Scholar]
  • 209.Helke, D. M., and A. C. L. Wong. 1994. Survival and growth characteristics of Listeria monocytogenes and Salmonella typhimurium on stainless steel and Buna-N rubber. J. Food Prot. 57:963-968. [DOI] [PubMed] [Google Scholar]
  • 210.Higgins, C. S., S. M. Murtough, E. Williamson, S. J. Hiom, D. J. Payne, A. D. Russell, and T. R. Walsh. 2001. Resistance to antibiotics and biocides among nonfermenting gram-negative bacteria. Clin. Microbiol. Infect. 7:308-315. [DOI] [PubMed] [Google Scholar]
  • 211.Hilburn, J., B. S. Hammond, E. J. Fendler, and P. A. Groziak. 2003. Use of alcohol hand sanitizer as an infection control strategy in an acute care facility. Am. J. Infect. Control 31:109-116. [DOI] [PubMed] [Google Scholar]
  • 212.Hilton, M., J. M. Chen, C. Barry, M. Vearncombe, and A. Simor. 2002. Deoxyribonucleic acid fingerprinting in an outbreak of Staphylococcus aureus intracranial infection after neurotologic surgery. Otol. Neurotol. 23:550-554. [DOI] [PubMed] [Google Scholar]
  • 213.Hingst, V., I. Juditzki, P. Heeg, and H.-G. Sonntag. 1992. Evaluation of the efficacy of surgical hand disinfection following a reduced application time of 3 instead of 5 min. J. Hosp. Infect. 20:79-86. [DOI] [PubMed] [Google Scholar]
  • 214.Hiom, S. J., J. R. Furr, A. D. Russell, and J. R. Dickinson. 1992. Effects of chlorhexidine diacetate on Candida albicans. C. glabrata and Saccharomyces cerevisiae. J. Appl. Bacteriol. 72:335-340. [DOI] [PubMed] [Google Scholar]
  • 215.Hoang, T. T., and H. P. Schweizer. 1999. Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis. J. Bacteriol. 181:5489-5497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 216.Hobson, R. P. 2003. The global epidemiology of invasive Candida infections—is the tide turning? J. Hosp. Infect. 55:159-168. [DOI] [PubMed] [Google Scholar]
  • 217.Hollenbeak, C. S., D. Murphy, W. C. Dunagan, and V. J. Fraser. 2002. Nonrandom selection and the attributable cost of surgical-site infections. Infect. Control Hosp. Epidemiol. 23:177-182. [DOI] [PubMed] [Google Scholar]
  • 218.Holloway, P. M., J. H. Platt, G. Reybrouck, H. A. Lilly, S. Mehtar, and Y. Drabu. 1990. A multi-centre evaluation of two chlorhexidine-containing formulations for surgical hand disinfection. J. Hosp. Infect. 16:151-159. [DOI] [PubMed] [Google Scholar]
  • 219.Hsueh, P. R., L. J. Teng, P. C. Yang, H. L. Pan, S. W. Ho, and K. T. Luh. 1999. Nosocomial pseudoepidemic caused by Bacillus cereus traced to contaminated ethyl alcohol from a liquor factory. J. Clin. Microbiol. 37:2280-2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 220.Huang, Y., S. Oie, and A. Kamiya. 1994. Comparative effectiveness of hand-cleansing agents for removing methicillin-resistant Staphylococcus aureus from experimentally contaminated fingertips. Am. J. Infect. Control 22:224-227. [DOI] [PubMed] [Google Scholar]
  • 221.Huang, Y.-C., T.-Y. Lin, H.-S. Leu, J.-L. Wu, and J. H. Wu. 1998. Yeast carriage on hands of hospital personnel working in intensive care units. J. Hosp. Infect. 39:47-51. [DOI] [PubMed] [Google Scholar]
  • 222.Hugo, W. B. 1979. Phenols: a review of their history and development as antimicrobial agents. Microbios 23:83-85. [PubMed] [Google Scholar]
  • 223.Hugonnet, S., T. V. Perneger, and D. Pittet. 2002. Alcohol-based handrub improves compliance with hand hygiene in intensive care units. Arch. Intern. Med. 162:1037-1043. [DOI] [PubMed] [Google Scholar]
  • 224.Hutto, C., E. A. Little, R. Ricks, J. D. Lee, and R. F. Pass. 1986. Isolation of cytomegalovirus from toys and hands in a day care center. J. Infect. Dis. 154:527-530. [DOI] [PubMed] [Google Scholar]
  • 225.Isaacs, D., H. Dickson, C. O'Callaghan, R. Sheaves, A. Winter, and E. R. Moxon. 1991. Handwashing and cohorting in prevention of hospital-acquired infections with respiratory syncytial virus. Arch. Dis. Child. 66:227-231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 226.Isenberg, H. D., V. Tucci, F. Cintron, C. Singer, G. S. Weinstein, and D. H. Tyras. 1989. Single-source outbreak of Candida tropicalis complicating coronary bypass surgery. J. Clin. Microbiol. 27:2426-2428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 227.Ismaeel, N., T. El-Moug, J. R. Furr, and A. D. Russell. 1986. Resistance of Providencia stuartii to chlorhexidine: a consideration of the role of the inner membrane. J. Appl. Bacteriol. 60:361-367. [DOI] [PubMed] [Google Scholar]
  • 228.Ismaeel, N., J. R. Furr, and A. D. Russell. 1986. Sensitivity and resistance of some strains of Providencia stuartii to antiseptics, disinfectants and preservatives. Microbios Lett. 33:59-64. [Google Scholar]
  • 229.Isquith, A. Y., and W. R. Chesbro. 1963. Pools confluxes and transport of amino acids in Streptococcus faecium. Biochim. Biophys. Acta 74:642-658. [DOI] [PubMed] [Google Scholar]
  • 230.Jacques, L., D. Mathieu, F. Baumann, and A. Roussel. 1983. Bacterial study of the hands and the use of soap in the hospital environment. Biomed. Pharmacother. 37:415-418. [PubMed] [Google Scholar]
  • 231.Järvinen, H., J. Tenovuo, and P. Huovinen. 1993. In vitro susceptibility of Streptococcus mutans to chlorhexidine and six other antimicrobial agents. Antimicrob. Agents Chemother. 37:1158-1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 232.Jarvis, W. R. 1996. Selected aspects of the socioeconomic impact of nosocomial infections: morbidity, costs, and prevention. Infect. Control Hosp. Epidemiol. 17:552-557. [DOI] [PubMed] [Google Scholar]
  • 233.Jawad, A., A. M. Snelling, J. Heritage, and P. M. Hawkey. 1996. Influence of relative humidity and suspending menstrua on survival of Acinetobacter spp. on dry surfaces. J. Clin. Microbiol. 34:2881-2887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 234.Jenney, A. W., G. A. Harrington, P. L. Russo, and D. W. Spelman. 2001. Cost of surgical site infections following coronary artery bypass surgery. A. N. Z. J. Surg. 71:662-664. [DOI] [PubMed] [Google Scholar]
  • 235.Jernigan, J. A., B. S. Lowry, F. G. Hayden, S. A. Kyger, B. P. Conway, D. H. Groschel, and B. M. Farr. 1993. Adenovirus type 8 epidemic keratoconjunctivitis in an eye clinic: risk factors and control. J. Infect. Dis. 167:1307-1313. [DOI] [PubMed] [Google Scholar]
  • 236.Jones, D. S., S. P. Gorman, D. F. McCafferty, and A. D. Woolfson. 1991. The effects of three non-antibiotic, antimicrobial agents on the surface hydrophobicity of certain micro-organisms evaluated by different methods. J. Appl. Microbiol. 71:218-227. [DOI] [PubMed] [Google Scholar]
  • 237.Jones, M. V., M. A. Wood, and T. M. Herd. 1992. Comparative sensitivity of Vibrio cholerae O1 El Tor and Escherichia coli to disinfectants. Lett. Appl. Microbiol. 14:51-53. [Google Scholar]
  • 238.Jones, R. D., H. B. Jampani, J. L. Newman, and A. S. Lee. 2000. Triclosan: a review of effectiveness and safety in health care settings. Am. J. Infect. Control 28:184-196. [PubMed] [Google Scholar]
  • 239.Kagle, J., and A. G. Hay. 2002. Construction of a broad host range cloning vector conferring triclosan resistance. BioTechniques 33:491-492. [DOI] [PubMed] [Google Scholar]
  • 240.Kalmár, P., and R. H. Steinhagen. 1984. Chirurgische Händedesinfektion mit alkoholischen Einreibepräparaten. Eine Standortbestimmung. Chirurg 55:280-287. [PubMed] [Google Scholar]
  • 241.Kamm, O. 1921. The relation between structure and physiologic action of the alcohols. J. Am. Pharm. Assoc. 10:87-92. [Google Scholar]
  • 242.Kampf, G. 2004. The six golden rules to improve compliance in hand hygiene. J. Hosp. Infect. 56:S3-S5. [DOI] [PubMed] [Google Scholar]
  • 243.Kampf, G. 2003. State-of-the-art hand hygiene in community medicine. Int. J. Hyg. Environ. Health 206:465-472. [DOI] [PubMed] [Google Scholar]
  • 244.Kampf, G. 2004. Wirksamkeit ethanolischer Händedesinfektionsmittel gegenüber dem felinen Calicivirus (FCV) im praxisnahen Versuch. Krankenhaushyg. Infektionsverhut. 26:11-14. [Google Scholar]
  • 245.Kampf, G., P. Gastmeier, N. Wischnewski, J. Schlingmann, M. Schumacher, F. Daschner, and H. Rüden. 1996. Nosokomiale Infektionen in Deutschland—Erfassung und Prävention. NIDEP-Studie. 1. Zur Prävalenz in der Chirurgie. Chirurg 67:637-642. [PubMed] [Google Scholar]
  • 246.Kampf, G., M. Höfer, and H. Rüden. 1998. Inaktivierung von Chlorhexidin bei der in vitro Desinfektionsmitteltestung. Zentbl. Hyg. Umweltmed. 200:457-464. [PubMed] [Google Scholar]
  • 247.Kampf, G., M. Höfer, and C. Wendt. 1999. Efficacy of hand disinfectants against vancomycin-resistant enterococci in vitro. J. Hosp. Infect. 42:143-150. [DOI] [PubMed] [Google Scholar]
  • 248.Kampf, G., and A. Hollingsworth. 2003. Validity of the four European test strains of prEN 12054 for the determination of comprehensive bactericidal activity of an alcohol-based hand rub. J. Hosp. Infect. 55:226-231. [DOI] [PubMed] [Google Scholar]
  • 249.Kampf, G., R. Jarosch, and H. Rüden. 1998. Limited effectiveness of chlorhexidine based hand disinfectants against methicillin-resistant Staphylococcus aureus (MRSA). J. Hosp. Infect. 38:297-303. [DOI] [PubMed] [Google Scholar]
  • 250.Kampf, G., R. Jarosch, and H. Rüden. 1997. Wirksamkeit alkoholischer Händedesinfektionsmittel gegenüber Methicillin-resistenten Staphylococcus aureus (MRSA). Chirurg 68:264-270. [DOI] [PubMed] [Google Scholar]
  • 251.Kampf, G., and M. Kapella. 2003. Suitability of Sterillium Gel for surgical hand disinfection. J. Hosp. Infect. 54:222-225. [DOI] [PubMed] [Google Scholar]
  • 252.Kampf, G., and H. Löffler. 2003. Dermatological aspects of a successful introduction and continuation of alcohol-based hand rubs for hygienic hand disinfection. J. Hosp. Infect. 55:1-7. [DOI] [PubMed] [Google Scholar]
  • 253.Kampf, G., B. Meyer, and P. Goroncy-Bermes. 2003. Comparison of two test methods for the determination of sufficient antimicrobial efficacy of three different alcohol-based hand rubs for hygienic hand disinfection. J. Hosp. Infect. 55:220-225. [DOI] [PubMed] [Google Scholar]
  • 254.Kampf, G., and M. Muscatiello. 2003. Dermal tolerance of Sterillium, a propanol-based hand rub. J. Hosp. Infect. 55:295-298. [DOI] [PubMed] [Google Scholar]
  • 255.Kampf, G., M. Muscatiello, D. Häntschel, and M. Rudolf. 2002. Dermal tolerance and skin hydration properties of a new ethanol-based hand gel. J. Hosp. Infect. 52:297-301. [DOI] [PubMed] [Google Scholar]
  • 256.Kampf, G., and C. Ostermeyer. 2003. Inter-laboratory reproducibility of the EN 1500 reference hand disinfection. J. Hosp. Infect. 53:304-306. [DOI] [PubMed] [Google Scholar]
  • 257.Kampf, G., and C. Ostermeyer. 2002. Intra-laboratory reproducibility of the hand hygiene reference procedures of EN 1499 (hygienic hand wash) and EN 1500 (hygienic hand disinfection). J. Hosp. Infect. 52:219-224. [DOI] [PubMed] [Google Scholar]
  • 258.Kampf, G., M. Rudolf, J.-C. Labadie, and S. Barrett. 2002. Spectrum of antimicrobial activity and user acceptability of the hand disinfectant agent Sterillium Gel. J. Hosp. Infect. 52:141-147. [DOI] [PubMed] [Google Scholar]
  • 259.Kampf, G., M. Schumacher, F. Daschner, and H. Rüden. 1996. Postoperative Wundinfektionen in der Chirurgie—Prävalenz in Deutschland (NIDEP-Studie). Langenbecks Arch. Chir. 113:698-703. [PubMed] [Google Scholar]
  • 260.Kampf, G., N. Wischnewski, G. Schulgen, M. Schumacher, and F. Daschner. 1998. Prevalence and risk factors for nosocomial lower respiratory tract infections in German hospitals. J. Clin. Epidemiol. 51:485-502. [DOI] [PubMed] [Google Scholar]
  • 261.Kaplan, L. M., and M. McGuckin. 1986. Increasing handwashing compliance with more accessible sinks. Am. J. Infect. Control 7:408-410. [DOI] [PubMed] [Google Scholar]
  • 262.Kewitsch, A., and W. Weuffen. 1970. Wirkung chemischer Desinfektionsmittel gegenüber Influenza-, Vaccinia- und Poliomyelitisvirus. Z. Gesamte Hyg. 16:687-691. [PubMed] [Google Scholar]
  • 263.Khanna, N., D. Goldenbèrger, P. Graber, M. Battegay, and A. F. Widmer. 2003. Gastroenteritis outbreak with norovirus in a Swiss university hospital with a newly identified virus strain. J. Hosp. Infect. 55:131-136. [DOI] [PubMed] [Google Scholar]
  • 264.Khatib, M., G. Jamaleddine, A. Abdallah, and Y. Ibrahim. 1999. Hand washing and use of gloves while managing patients receiving mechanical ventilation in the ICU. Chest 116:172-175. [DOI] [PubMed] [Google Scholar]
  • 265.Kim, J. M., E. S. Park, J. S. Jeong, K. M. Kim, J. M. Kim, H. S. Oh, S. W. Yoon, H. S. Chang, S. I. Lee, M. S. Lee, J. H. Song, M. W. Kang, S. C. Park, K. W. Choe, and C. H. Pal. 2000. Multicenter surveillance study for nosocomial infections in major hospitals in Korea. Nosocomial infection surveillance committee of the Korean Society for Nosocomial Infection Control. Am. J. Infect. Control 28:454-458. [DOI] [PubMed] [Google Scholar]
  • 266.Kirkland, K. B., and J. M. Weinstein. 1999. Adverse effects of contact isolation. Lancet 354:1177-1178. [DOI] [PubMed] [Google Scholar]
  • 267.Kjølen, H., and B. M. Andersen. 1992. Handwashing and disinfection of heavily contaminated hands—effective or ineffective? J. Hosp. Infect. 21:61-71. [DOI] [PubMed] [Google Scholar]
  • 268.Klein, M., and A. Deforest. 1963. Antiviral action of germicides. Soap Chem. Spec. 39:70-72. [Google Scholar]
  • 269.Klemperer, R. M. M., N. T. A. J. Ismail, and M. R. W. Brown. 1980. Effect of R-plasmid RP1 and nutrient depletion on the resistance of Escherichia coli to cetremide, chlorhexidine and phenol. J. App. Bacteriol. 48:349-357. [DOI] [PubMed] [Google Scholar]
  • 270.Knight, B. A., R. Puy, J. Douglass, R. E. O'Hehir, and F. Thien. 2001. Chlorhexidine anaphylaxis: a case report and review of the literature. Intern. Med. J. 31:436-437. [DOI] [PubMed] [Google Scholar]
  • 271.Knittle, M. A., D. V. Eitzman, and H. Baer. 1975. Role of hand contamination of personnel in the epidemiology of gram-negative nosocomial infections. J. Pediatr. 86:433-437. [DOI] [PubMed] [Google Scholar]
  • 272.Kobayashi, H., M. Tsuzuki, and K. Koshimizu. 1984. Susceptibility of hepatitis B virus to disinfectants or heat. J. Clin. Microbiol. 20:214-216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 273.Koch, R. 1888. Über Desinfektion. Mitt. Kaiserlich. Gesundheits. Berlin 1:234-282. [Google Scholar]
  • 274.Kohlbecker, G. 1989. Toxic impurities in chlorhexidine digluconate. Dsch. Zahnärztl. Z. 44:273-276. [PubMed] [Google Scholar]
  • 275.Kownatzki, E. 2003. Hand hygiene and skin health. J. Hosp. Infect. 55:239-245. [DOI] [PubMed] [Google Scholar]
  • 276.Kralj, N., M. Beie, and F. Hofmann. 1999. Surgical gloves — how well do they protect against infections? Gesundheitswesen 61:398-403. [PubMed] [Google Scholar]
  • 277.Kramer, A. 1977. Hahnekammepidermophytie- und Kandidosetests im System der Screening-Testung für antifungiell wirksame Substanzen. Ernst-Moritz-Arndt University, Greifswald, Germany.
  • 278.Kramer, A., V. Adrian, P. Rudolph, S. Wurster, and H. Lippert. 1998. Explant test with skin and peritoneum of the neonatal rat as a predictive test of tolerance of local anti-infective agents in wounds and body cavities. Chirurg 69:840-845. [DOI] [PubMed] [Google Scholar]
  • 279.Kramer, A., T. Bernig, and G. Kampf. 2002. Clinical double-blind trial on the dermal tolerance and user acceptability of six alcohol-based hand disinfectants for hygienic hand disinfection. J. Hosp. Infect. 51:114-120. [DOI] [PubMed] [Google Scholar]
  • 280.Kramer, A., V. Mersch-Sundermann, H. Gerdes, F.-A. Pitten, and H. Tronnier. 2003. Toxikologische Bewertung für die Händedesinfektion relevanter antimikrobieller Wirkstoffe, p. 105-174. In G. Kampf (ed.), Hände-Hygiene im Gesundheitswesen. Springer-Verlag KG, Berlin, Germany.
  • 281.Kramer, A., and P. Rudolph. 2002. Efficacy and tolerance of selected antiseptic substances in respect of suitability for use on the eye, p. 117-144. In A. Kramer and W. Behrens-Baumann (ed.), Antiseptic prophylaxis and therapy in ocular infections, vol. 33. Karger, Basel, Switzerland. [DOI] [PubMed]
  • 282.Kramer, A., P. Rudolph, G. Kampf, and D. Pittet. 2002. Limited efficacy of alcohol-based hand gels. Lancet 359:1489-1490. [DOI] [PubMed] [Google Scholar]
  • 283.Kramer, A., W. Weuffen, and W. Schwenke. 1973. Mikrobiologische und dermatologische Anforderungen an antiseptische Seifen. Dermatol. Monatsschr. 159:526-539. [PubMed] [Google Scholar]
  • 284.Krivlov, L. R., and S. H. Harkness. 1993. Inactivation of respiratory syncytial virus by detergents and disinfectants. Pediatr. Infect. Dis. J. 12:582-584. [DOI] [PubMed] [Google Scholar]
  • 285.Kruse, R. H., T. D. Green, and B. C. Chambers. 1963. Disinfection of aerosolized pathogenic fungi on laboratory surfaces. I. Tissue phase. Appl. Microbiol. 11:436-445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 286.Kruse, R. H., T. D. Green, and B. C. Chambers. 1964. Disinfection of aerosolized pathogenic fungi on laboratory surfaces. II. Culture phase. Appl. Microbiol. 12:155-160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 287.Kurtz, J. B. 1979. Virucidal effect of alcohols against echovirus 11. Lancet i:496-497. [DOI] [PubMed] [Google Scholar]
  • 288.Kurtz, J. B., T. W. Lee, and A. J. Parsons. 1980. The action of alcohols on rotavirus, astrovirus and enterovirus. J. Hosp. Infect. 1:321-325. [DOI] [PubMed] [Google Scholar]
  • 289.Kyne, L., M. B. Hamel, R. Polavaram, and C. P. Kelly. 2002. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin. Infect. Dis. 34:346-353. [DOI] [PubMed] [Google Scholar]
  • 290.Lambert, R. J., J. Joynson, and B. Forbes. 2001. The relationship and susceptibilities of some industrial laboratory and clinical isolates of Pseudomonas aeruginosa to some antibiotics and biocides. J. Appl. Microbiol. 91:972-984. [DOI] [PubMed] [Google Scholar]
  • 291.Lannigan, R., and L. E. Bryan. 1985. Decreased susceptibility of Serratia marcescens to chlorhexidine related to the inner membrane. J. Antimicrob. Chemother. 15:559-565. [DOI] [PubMed] [Google Scholar]
  • 292.Lark, R. L., K. VanderHyde, G. M. Deeb, S. Dietrich, J. P. Massey, and C. Chenoweth. 2001. An outbreak of coagulase-negative staphylococcal surgical-site infections following aortic valve replacement. Infect. Control Hosp. Epidemiol. 22:618-623. [DOI] [PubMed] [Google Scholar]
  • 293.Larson, E. 1983. Compliance with isolation technique. Am. J. Infect. Control 11:221-225. [DOI] [PubMed] [Google Scholar]
  • 294.Larson, E. 1984. Effects of handwashing agent, handwashing frequency, and clinical area on hand flora. Am. J. Infect. Control 11:76-82. [DOI] [PubMed] [Google Scholar]
  • 295.Larson, E., A. Aiello, L. V. Lee, P. Della-Latta, C. Gomez-Duarte, and S. Lin. 2003. Short- and long-term effects of handwashing with antimicrobial or plain soap in the community. J. Commun. Health 28:139-150. [DOI] [PubMed] [Google Scholar]
  • 296.Larson, E., J. K. Anderson, and L. Baxendale. 1993. Effects of a protective foam on scrubbing and gloving. Am. J. Infect. Control 21:297-301. [DOI] [PubMed] [Google Scholar]
  • 297.Larson, E., and L. Bobo. 1992. Effective hand degerming in the presence of blood. J. Emerg. Med. 10:7-11. [DOI] [PubMed] [Google Scholar]
  • 298.Larson, E., C. Friedman, J. Cohran, J. Treston-Aurand, and S. Green. 1997. Prevalence and correlates of skin damage on the hands of nurses. Heart Lung 26:404-412. [DOI] [PubMed] [Google Scholar]
  • 299.Larson, E., J. J. Leyden, K. J. McGinley, G. L. Grove, and G. H. Talbot. 1986. Physiologic and microbiologic changes in skin related to frequent handwashing. Infect. Control 7:59-63. [DOI] [PubMed] [Google Scholar]
  • 300.Larson, E., K. J. McGinley, G. L. Grove, J. J. Leyden, and G. H. Talbot. 1986. Physiologic, microbiologic, and seasonal effects of handwashing on the skin of health care presonnel. Am. J. Infect. Control 14:51-59. [DOI] [PubMed] [Google Scholar]
  • 301.Larson, E., M. Silberger, K. Jakob, S. Whittier, L. Lai, P. Della Latta, and L. Saiman. 2000. Assessment of alternative hand hygiene regimes to improve skin health among neonatal intensive care unit nurses. Heart Lung 29:136-142. [PubMed] [Google Scholar]
  • 302.Larson, E. L. 1981. Persistant carriage of gram-negative bacteria on hands. Am. J. Infect. Control 9:112-119. [DOI] [PubMed] [Google Scholar]
  • 303.Larson, E. L., A. E. Aiello, J. Bastyr, C. Lyle, J. Stahl, A. Cronquist, L. Lai, and P. Della-Latta. 2001. Assessment of two hand hygiene regimes for intensive care unit personnel. Crit. Care Med. 29:944-951. [DOI] [PubMed] [Google Scholar]
  • 304.Larson, E. L., A. E. Aiello, J. M. Heilman, C. T. Lyle, A. Cronquist, and J. B. Stahl. 2001. Comparison of different regimes for surgical hand preparation. AORN J. 73:412-420. [DOI] [PubMed] [Google Scholar]
  • 305.Larson, E. L., A. M. Butz, D. L. Gullette, and B. A. Laughon. 1990. Alcohol for surgical scrubbing? Infect. Control Hosp. Epidemiol. 11:139-143. [DOI] [PubMed] [Google Scholar]
  • 306.Larson, E. L., P. I. Eke, and B. E. Laughon. 1986. Efficacy of alcohol-based hand rinses under frequent-use conditions. Antimicrob. Agents Chemother. 30:542-544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 307.Larson, E. L., C. Gomez-Duarte, L. V. Lee, P. Della-Latta, D. J. Kain, and B. H. Keswick. 2002. Microbial flora of hands of homemakers. Am. J. Infect. Control 31:72-79. [DOI] [PubMed] [Google Scholar]
  • 308.Larson, E. L., K. J. McGinley, A. Foglia, J. J. Leyden, N. Boland, J. Larson, L. C. Altobelli, and E. Salazar-Lindo. 1992. Handwashing practices and resistance and density of bacterial hand flora on two pediatric units in Lima, Peru. Am. J. Infect. Control 20:65-72. [DOI] [PubMed] [Google Scholar]
  • 309.Larson, E. L., C. A. Norton Hughes, J. D. Pyrak, S. M. Sparks, E. U. Cagatay, and J. M. Bartkus. 1998. Changes in bacterial flora associated with skin damage on hands of health care personnel. Am. J. Infect. Control 26:513-521. [DOI] [PubMed] [Google Scholar]
  • 310.Lasthein Andersen, B., and F. Brandrup. 1985. Contact dermatitis from chlorhexidine. Contact Dermatitis 13:307-309. [DOI] [PubMed] [Google Scholar]
  • 311.Lee, Y. L., T. Cesario, R. Lee, S. Nothvogel, J. Nassar, N. Farsad, and L. Thrupp. 1994. Colonization by Staphylococcus species resistant to methicillin or quinolone on hands of medical personnel in a skilled-nursing facility. Am. J. Infect. Control 22:346-351. [DOI] [PubMed] [Google Scholar]
  • 312.Levy, C. W., A. Roujeinikova, S. Sedelnikova, P. J. Baker, A. R. Stuitje, A. R. Slabas, D. W. Rice, and J. B. Rafferty. 1999. Molecular basis of triclosan activity. Nature 398:383-384. [DOI] [PubMed] [Google Scholar]
  • 313.Levy, S. B. 2002. Active efflux, a common mechanism for biocide and antibiotic resistance. J. Appl. Microbiol. 92:65S-71S. [PubMed] [Google Scholar]
  • 314.Levy, S. B. 2001. Antibacterial household products: cause for concern. Emerg. Infect. Dis. 7:512-515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 315.Leyden, J. J., and K. J. McGinley. 1993. Coryneform bacteria, p. 102-117. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 316.Leyden, J. J., K. J. McGinley, M. S. Kaminer, J. Bakel, S. Nishijima, M. J. Grove, and G. L. Grove. 1991. Computerized image analysis of full-hand touch plates: a method for quantification of surface bacteria on hands and the effect of antimicrobial agents. J. Hosp. Infect. 18:13-22. [DOI] [PubMed] [Google Scholar]
  • 317.Lilly, H. A., E. J. Lowbury, and M. D. Wilkins. 1979. Limits to progressive reduction of resident skin bacteria by disinfection. J. Clin. Pathol. 32:382-385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 318.Lilly, H. A., and E. J. L. Lowbury. 1978. Transient skin flora—their removal by cleansing or disinfection in relation to their mode of deposition. J. Clin. Pathol. 31:919-922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 319.Lilly, H. A., E. J. L. Lowbury, and M. D. Wilkins. 1979. Detergents compared with each other and with antiseptics as skin ‘degerming’ agents. J. Hyg. (Cambridge) 82:89-93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 320.Lilly, H. A., E. J. L. Lowbury, M. D. Wilkins, and A. Zaggy. 1979. Delayed antimicrobial effects of skin disinfection by alcohol. J. Hyg. (Cambridge) 82:497-500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 321.Linton, K. B., and E. George. 1966. Inactivation of chlorhexidine (‘Hibitane’) by bark corks. Lancet i:1353-1355. [DOI] [PubMed] [Google Scholar]
  • 322.Lockemann, G., F. Bär, and W. Totzeck. 1941. Über die keimtötende Wirkung von Alkoholen. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. A 147:1-15. [Google Scholar]
  • 323.Lockhart, J. 1972. How toxic is hexachlorophen? Pediatrics 50:229-235. [PubMed] [Google Scholar]
  • 324.Lohr, J. A., D. L. Ingram, S. M. Dudley, E. L. Lawton, and L. G. Donowitz. 1991. Hand washing in pediatric ambulatory settings. Am. J. Dis. Child. 145:1198-1199. [DOI] [PubMed] [Google Scholar]
  • 325.Lowbury, E. J. L. 1969. Gram-negative bacilli on the skin. Br. J. Dermatol. 81:55-61. [DOI] [PubMed] [Google Scholar]
  • 326.Lowbury, E. J. L., and H. A. Lilly. 1960. Disinfection of the hands of surgeons and nurses. Br. Med. J. 1:1445-1450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 327.Lowbury, E. J. L., and H. A. Lilly. 1973. Use of 4% chlorhexidine detergent solution (Hibiscrub) and other methods of skin disinfection. Br. Med. J. 1:510-515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 328.Lowbury, E. J. L., H. A. Lilly, and G. A. J. Ayliffe. 1974. Preoperative disinfections of surgeons' hands: use of alcoholic solutions and effects of gloves on skin flora. Br. Med. J. 4:369-372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 329.Lowbury, E. J. L., H. A. Lilly, and J. P. Bull. 1963. Disinfection of hands: removal of resident bacteria. Br. Med. J. 1:1251-1256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 330.Lowbury, E. J. L., H. A. Lilly, and J. P. Bull. 1964. Disinfection of hands: removal of transient organisms. Br. Med. J. 2:230-233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 331.Lowenthal, K. 1961. The antifungal effect of 70% ethyl alcohol. Arch. Dermatol. 83:803-805. [DOI] [PubMed] [Google Scholar]
  • 332.Lübbe, J., C. Ruffieux, and D. Perrenoud. 2000. A stinging cause for preventive skin care. Lancet 356:768-769. [DOI] [PubMed] [Google Scholar]
  • 333.Lübbe, J., C. Ruffieux, G. van Melle, and D. Perrenoud. 2001. Irritancy of the skin disinfectant n-propanol. Contact Dermatitis 45:226-231. [DOI] [PubMed] [Google Scholar]
  • 334.Lund, S., J. Jackson, J. Leggett, L. Hales, R. Dworkin, and D. Gilbert. 1994. Reality of glove use and handwashing in a community hospital. Am. J. Infect. Control 22:352-357. [DOI] [PubMed] [Google Scholar]
  • 335.Lyytikainen, O., S. Koljalg, M. Harma, and J. Vuopio-Varkila. 1995. Outbreak caused by two multi-resistant Acinetobacter baumannii clones in a burns unit: emergence of resistance to imipenem. J. Hosp. Infect. 31:41-54. [DOI] [PubMed] [Google Scholar]
  • 336.MacDonald, A., F. Dinah, D. MacKenzie, and A. Wilson. 2004. Performance feedback of hand hygiene, using alcohol gel as the skin decontaminant, reduces the number of inpatients newly affected by MRSA and antibiotic costs. J. Hosp. Infect. 56:56-63. [DOI] [PubMed] [Google Scholar]
  • 337.Mäkela, P. 1993. Gesunde Haut als Voraussetzung für eine effektive Händedesinfektion, p. 97-103. In A. Kramer, D. Gröschel, P. Heeg, H. Lippert, M. Rotter, and W. Weuffen (ed.), Klinische Antiseptik. Springer-Verlag KG, Berlin, Germany.
  • 338.Maki, D. 1978. Control of colonization and transmission of pathogenic bacteria in the hospital. Ann. Intern. Med. 89:777-780. [DOI] [PubMed] [Google Scholar]
  • 339.Maki, D. G. 1989. The use of antiseptics for handwashing by medical personnel. J. Chemother. 1:3-11. [DOI] [PubMed] [Google Scholar]
  • 340.Malik, R. K., M. A. Montecalvo, M. R. Reale, K. Li, M. Maw, J. L. Munoz, C. Gedris, K. van Horn, K. A. Carnevale, M. H. Levi, and H. S. Dweck. 1999. Epidemiology and control of vancomycin-resistant enterococci in a regional neonatal intensive care unit. Pediatr. Infect. Dis. J. 18:352-356. [DOI] [PubMed] [Google Scholar]
  • 341.Marchetti, M. G., G. Kampf, G. Finzi, and G. Salvatorelli. 2003. Evaluation of the bactericidal effect of five products for surgical hand disinfection according to prEN 12054 and prEN 12791. J. Hosp. Infect. 54:63-67. [DOI] [PubMed] [Google Scholar]
  • 342.Marchetti, O., J. Bille, U. Fluckiger, P. Eggimann, C. Ruef, J. Garbino, J. Calandra, M. P. Glauser, M. G. Tauber, and D. Pittet. 2004. Epidemiology of candidemia in Swiss tertiary care hospitals: secular trends, 1991-2000. Clin. Infect. Dis. 38:311-320. [DOI] [PubMed] [Google Scholar]
  • 343.Marena, C., L. Lodola, M. Zecca, A. Bulgheroni, E. Carretto, X. Maserati, and L. Zambianchi. 2002. Assessment of handwashing practices with chemical and microbiological methods: preliminary results from a prospective crossover study. Am. J. Infect. Control 30:334-340. [DOI] [PubMed] [Google Scholar]
  • 344.Marples, R. R., and A. G. Towers. 1979. A laboratory model for the investigation of contact transfer of microorganisms. J. Hyg. (Cambridge) 82:237-248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 345.Marrie, T. J., and J. W. Costerton. 1981. Proplonged survival of Serratia marcescens in chlorhexidine. Appl. Environ. Microbiol. 42:1093-1102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 346.Martin, L. S., J. S. Meoougal, and S. L. Loskoski. 1985. Disinfection and inactivation of the human T lymphotropic virus type III/lymphadenopathy associated virus. J. Infect. Dis. 152:400-403. [DOI] [PubMed] [Google Scholar]
  • 347.Martone, W. J. 1998. Spread of vancomycin-resistant enterococci: why did it happen in the United States? Infect. Control Hosp. Epidemiol. 19:539-545. [DOI] [PubMed] [Google Scholar]
  • 348.Martone, W. J., O. C. Tablan, and W. R. Jarvis. 1987. The epidemiology of nosocomial epidemic Pseudomonas cepacia infections. Eur. J. Epidemiol. 3:222-232. [DOI] [PubMed] [Google Scholar]
  • 349.Massanari, R. M., and W. J. Hierholzer. 1984. A crossover comparison of antiseptic soaps on nosocomial infection rates in intensive care units. Am. J. Infect. Control 12:247-248. [Google Scholar]
  • 350.Maule, A. 2000. Survival of verocytotoxigenic Escherichia coli O157 in soil, water and on surfaces. Symp. Seri. (Soci. Appl. Microbiol.) 29:71S-78S. [DOI] [PubMed] [Google Scholar]
  • 351.Maury, E., M. Alzieu, J. L. Baudel, N. Haram, F. Barbut, B. Guidet, and G. Offenstadt. 2000. Availability of an alcohol solution can improve hand disinfection compliance in an intensive care unit. Am. J. Respir. Crit. Care Med. 162:324-327. [DOI] [PubMed] [Google Scholar]
  • 352.Mayer, J. A., P. M. Dubbert, M. Miller, P. A. Burkett, and S. W. Chapman. 1986. Increasing handwashing in an intensive care unit. Am. J. Infect. Control 7:259-262. [DOI] [PubMed] [Google Scholar]
  • 353.Mayon-White, R. T., G. Ducel, T. Kereselidze, and E. Tikomirov. 1988. An international survey of the prevalence of hospital-acquired infection. J. Hosp. Infect. 11:43-48. [DOI] [PubMed] [Google Scholar]
  • 354.Mbithi, J. N., V. S. Springthorpe, J. R. Boulet, and S. A. Sattar. 1992. Survival of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces. J. Clin. Microbiol. 30:757-763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 355.Mbithi, J. N., V. S. Springthorpe, and S. A. Sattar. 1993. Comparative in vivo efficiencies of hand-washing agents against hepatitis A virus (HM-175) and poliovirus type 1 (Sabin). Appl. Environ. Microbiol. 59:3463-3469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 356.Mbithi, J. N., V. S. Springthorpe, and S. A. Sattar. 1991. Effect of relative humidity and air temperature on survival of hepatitis A virus on environmental surfaces. Appl. Environ. Microbiol. 57:1394-1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 357.McAllister, T. A., C. E. Lucas, H. Mocan, R. H. A. Liddell, B. E. S. Gibson, I. M. Hann, and D. J. Platt. 1989. Serratia marcescens outbreak in a paediatric oncology unit traced to contaminated chlorhexidine. Scott. Med. J. 34:525-528. [DOI] [PubMed] [Google Scholar]
  • 358.McBride, M. E., W. C. Duncan, and J. M. Knox. 1975. Physiological and environmental control of Gram negative bacteria on skin. Brit. J. Dermatol. 93:191-199. [DOI] [PubMed] [Google Scholar]
  • 359.McBride, M. E., L. F. Montes, W. J. Fahlberg, and J. M. Knox. 1975. Microbial flora of nurses' hands. III. The relationship between staphylococcal skin populations and persistence of carriage. Int. J. Dermatol. 14:129-135. [DOI] [PubMed] [Google Scholar]
  • 360.McDonnell, G., and A. D. Russell. 1999. Antiseptics and disinfectants: activity, action, resistance. Clin. Microbiol. Rev. 12:147-179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 361.McEwan, P., and D. Jenkins. 1993. The basis of the skin surface ecosystem, p. 1-32. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 362.McFarland, L. V., M. E. Mulligan, R. Y. Y. Kwok, and W. E. Stamm. 1989. Nosocomial acquisition of Clostridium difficile infection. N. Engl. J. Med. 320:204-210. [DOI] [PubMed] [Google Scholar]
  • 363.McFarland, L. V., and W. E. Stamm. 1986. Review of Clostridium difficile-associated diseases. Am. J. Infect. Control 14:99-109. [DOI] [PubMed] [Google Scholar]
  • 364.McLaws, M.-L., and P. C. Taylor. 2003. The hospital infection standardised surveillance (HISS) programme: analysis of a two-year pilot. J. Hosp. Infect. 53:259-267. [DOI] [PubMed] [Google Scholar]
  • 365.McMurry, L. M., P. F. McDermott, and S. B. Levy. 1999. Genetic evidence that inhA of Mycobacterium smegmatis is a target for triclosan. Antimicrob. Agents Chemother. 43:711-713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 366.McMurry, L. M., M. Oethinger, and S. B. Levy. 1998. Overexpression of marA. soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol. Lett. 166:305-309. [DOI] [PubMed] [Google Scholar]
  • 367.McMurry, L. M., M. Oethinger, and S. B. Levy. 1998. Triclosan targets lipid synthesis. Nature 394:531-532. [DOI] [PubMed] [Google Scholar]
  • 368.McNeil, S. A., C. L. Foster, S. A. Hedderwick, and C. A. Kauffman. 2001. Effect of hand cleansing with antimicrobial soap or alcohol-based gel on microbial colonization of artificial fingernails worn by healthcare workers. Clin. Infect. Dis. 32:367-372. [DOI] [PubMed] [Google Scholar]
  • 369.Meade, M. J., R. L. Waddell, and T. M. Callahan. 2001. Soil bacteria Pseudomonas putida and Alcaligenes xylosoxidans subsp. denitrificans inactivate triclosan in liquid and solid substrates. FEMS, Microbiol. Lett. 204:45-48. [DOI] [PubMed] [Google Scholar]
  • 370.Meengs, M. R., B. K. Giles, C. D. Chisholm, W. H. Cordell, and D. R. Nelson. 1994. Hand washing frequency in an emergency department. Ann. Emerg. Med. 23:1307-1312. [DOI] [PubMed] [Google Scholar]
  • 371.Meers, P. D., and G. A. Yeo. 1978. Shedding of bacteria and skin squames after handwashing. J. Hyg. (London) 81:99-105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 372.Meinche, B. E., R. G. Kranz, and D. L. Lynch. 1980. Effect of irgasan on bacterial growth and its adsorption into the cell wall. Microbios 28:133-147. [PubMed] [Google Scholar]
  • 373.Merry, A. F., T. E. Miller, G. Findon, C. S. Webster, and S. P. Neff. 2001. Touch contamination levels during anaesthetic procedures and their relationship to hand hygiene procedures. Br. J. Anaesthesiol. 87:291-294. [DOI] [PubMed] [Google Scholar]
  • 374.Miller, M. A., M. Hyland, M. Ofner-Agostini, M. Gourdeau, and M. Ishak. 2002. Morbidity, mortality, and healthcare burden of nosocomial Clostridium difficile-associated diarrhea in Canadian hospitals. Infect. Control Hosp. Epidemiol. 23:137-140. [DOI] [PubMed] [Google Scholar]
  • 375.Mims, C. A. 1988. The pathogenesis of infectious disease, 3rd ed. Academic Press, Ltd., London, United Kingdom.
  • 376.Mitscherlich, E., and E. H. Marth. 1984. Microbial survival in the environment. Springer-Verlag KG, Berlin, Germany.
  • 377.Mittermayer, H., and M. Rotter. 1975. Vergleich der Wirkung von Wasser, einigen Detergentien und Äthylalkohol auf die transiente Flora der Haut. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 160:163-172. [PubMed] [Google Scholar]
  • 378.Mody, L., S. A. McNeil, R. Sun, S. E. Bradley, and C. A. Kauffman. 2003. Introduction of a waterless alcohol-based hand rub in a long-term-care facility. Infect. Control Hosp. Epidemiol. 24:165-171. [DOI] [PubMed] [Google Scholar]
  • 379.Montes, L. F., and W. H. Wilborn. 1969. Location of bacterial skin flora. Br. J. Dermatol. 81:23-26. [DOI] [PubMed] [Google Scholar]
  • 380.Montessori, V., S. Scharf, S. Holland, D. H. Werker, F. J. Roberts, and E. Bryce. 1998. Epidemic keratoconjunctivitis outbreak at a tertiary referral eye care clinic. Am. J. Infect. Control 26:399-405. [DOI] [PubMed] [Google Scholar]
  • 381.Morris, A. M., B. A. Jobe, M. Stoney, B. C. Sheppard, C. W. Deveney, and K. E. Deveney. 2002. Clostridium difficile colitis: an increasingly aggressive iatrogenic disease? Arch. Surg. 137:1096-1100. [DOI] [PubMed] [Google Scholar]
  • 382.Morrison, A. J., J. Gratz, I. Cabezudo, and R. P. Wenzel. 1986. The efficacy of several new handwashing agents for removing non-transient bacterial flora from hands. Infect. Control 7:268-272. [DOI] [PubMed] [Google Scholar]
  • 383.Morton, H. W. 1950. Relationship of concentration and germicidal efficacy of ethyl alcohol. Ann. N. Y. Acad. Sci. 532:191-196. [DOI] [PubMed] [Google Scholar]
  • 384.Mulberry, G., A. T. Snyder, J. Heilman, J. Pyrek, and J. Stahl. 2001. Evaluation of a waterless, scrubless chlorhexidine gluconate/ethanol surgical scrub for antimicrobial efficacy. Am. J. Infect. Control 29:377-382. [DOI] [PubMed] [Google Scholar]
  • 385.Murray, B. E. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3:46-65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 386.Murray, J., and R. M. Calman. 1955. Control of cross-infection by means of an antiseptic hand cream. Brit. Med. J. 4905:81-83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 387.Musa, E. K., N. Desai, and M. W. Casewell. 1990. The survival of Acinetobacter calcoaceticus inoculated on fingertips and on formica. J. Hosp. Infect. 15:219-227. [DOI] [PubMed] [Google Scholar]
  • 388.Muto, C. A., M. G. Sistrom, and B. M. Farr. 2000. Hand hygiene rates unaffected by installation of dispensers of a rapidly acting hand antiseptic. Am. J. Infect. Control 28:273-276. [DOI] [PubMed] [Google Scholar]
  • 389.Nakahara, H., and H. Kozukoe. 1981. Chlorhexidine resistance in Escherichia coli isolated from clinical lesions. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 251:177-184. [PubMed] [Google Scholar]
  • 390.Nakahara, H., and H. Kozukue. 1982. Isolation of chlorhexidine-resistant Pseudomonas aeruginosa from clinical lesions. J. Clin. Microbiol. 15:166-168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 391.Narang, H. K., and A. A. Codd. 1983. Action of commonly used disinfectants against enteroviruses. J. Hosp. Infect. 4:209-212. [DOI] [PubMed] [Google Scholar]
  • 392.Naver, L. P., and F. Gottrup. 2000. Incidence of glove perforations in gastrointestinal surgery and the protective effect of double gloves: a prospective, randomised controlled study. Eur. J. Surg. 166:293-295. [DOI] [PubMed] [Google Scholar]
  • 393.Neely, A. N. 2000. A survey of gram-negative bacteria survival on hospital fabrics and plastics. J. Burn Care and Rehabil. 21:523-527. [DOI] [PubMed] [Google Scholar]
  • 394.Neely, A. N., and M. P. Maley. 2000. Survival of enterococci and staphylococci on hospital fabric and plastic. J. Clin. Microbiol. 38: 724-726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 395.Neufeld, F., and O. Schiemann. 1939. Über die Wirkung des Alkohols bei der Händedesinfektion. Z. Hyg. 121:312-333. [Google Scholar]
  • 396.Newman, J. L., and J. C. Seitz. 1990. Intermittent use of an antimicrobial hand gel for reducing soap-induced irritation of health care personnel. Am. J. Infect. Control 18:194-200. [DOI] [PubMed] [Google Scholar]
  • 397.Nicholls, T. M., and A. J. Morris. 1997. Nosocomial infections in Auckland Health-care hospitals. N. Z. Med. J. 110:314-316. [PubMed] [Google Scholar]
  • 398.Nicoletti, G., V. Boghossian, and R. Borland. 1990. Hygienic hand disinfection: a comparative study with chlorhexidine detergents and soap. J. Hosp. Infect. 15:323-337. [DOI] [PubMed] [Google Scholar]
  • 399.Noble, W. C. 1993. Other cutaneous bacteria, p. 210-231. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 400.Noble, W. C. 1993. Staphylococci as pathogens, p. 153-172. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 401.Noble, W. C. 1993. Staphylococci on the skin, p. 135-152. In W. C. Noble (ed.), The skin microflora and microbial skin disease. Cambridge University Press, Cambridge, United Kingdom.
  • 402.Noskin, G. A., V. Stosor, I. Cooper, and L. R. Peterson. 1995. Recovery of vancomycin-resistant enterococci on fingertips and environmental surfaces. Infect. Control Hosp. Epidemiol. 16:577-581. [DOI] [PubMed] [Google Scholar]
  • 403.Nystrom, B. 1994. Impact of handwashing on mortality in intensive care: examination of the evidence. Infect. Control Hosp. Epidemiol. 15:435-436. [DOI] [PubMed] [Google Scholar]
  • 404.O'Farrell, D. A., G. Kenny, M. O'Sullivan, P. Nicholson, M. Stephens, and R. Hone. 1994. Evaluation of the optimal hand-scrub duration prior to total hip arthroplasty. J. Hosp. Infect. 26:93-98. [DOI] [PubMed] [Google Scholar]
  • 405.Ohlenschlaeger, J., J. Friberg, D. Ramsing, and T. Agner. 1996. Temperature dependency of skin susceptibility to water and detergents. Acta Dermatol. Venereol. 76:274-276. [DOI] [PubMed] [Google Scholar]
  • 406.Ojajärvi, J. 1980. Effectiveness of hand washing and disinfection methods in removing transient bacteria after patient nursing. J. Hyg. (Cambridge) 85:193-203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 407.Ojajärvi, J. 1981. The importance of soap selection for routine hand hygiene in hospitals. J. Hyg. (Cambridge) 86:275-283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 408.Ojajärvi, J., P. Mälelä, and I. Rantasalo. 1977. Failure of hand disinfection with frequent hand washing: a need for prolonged field studies. J. Hyg. (London) 79:107-119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 409.Okano, M., M. Nomura, S. Hata, N. Okada, K. Sato, Y. Kitano, M. Tashiro, Y. Yoshimoto, R. Hama, and T. Aoki. 1989. Anaphylactic symtoms due to chlorhexidine gluconate. Arch. Dermatol. 125:50-52. [PubMed] [Google Scholar]
  • 410.Okuda, T., N. Endo, Y. Osada, and H. Zen-Yoji. 1984. Outbreak of nosocomial urinary tract infections caused by Serratia marcescens. J. Clin. Microbiol. 20:691-695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 411.Olaechea, P. M., M.-A. Ulibarrena, F. Álvarez-Lerma, J. Insausti, M. Palomar, and M.-A. de la Cal. 2003. Factors related to hospital stay among patients with nosocomial infection acquired in the intensive care unit. Infect. Control Hosp. Epidemiol. 24:207-213. [DOI] [PubMed] [Google Scholar]
  • 412.Opal, S. M., K. H. Mayer, M. J. Stenberg, J. E. Blazek, D. J. Mikolich, D. L. Dickensheets, L. W. Lyhte, R. R. Trudel, and J. M. Musser. 1990. Frequent acquisition of multiple strains of methicillin-resistant Staphylococcus aureus by healthcare workers in an endemic hospital environment. Infect. Control Hosp. Epidemiol. 11:479-485. [DOI] [PubMed] [Google Scholar]
  • 413.Ophaswongse, S., and H. I. Maibach. 1994. Alcohol dermatitis: allergic contact dermatitis and contact urticaria syndrome. Contact Dermatitis 30:1-6. [DOI] [PubMed] [Google Scholar]
  • 414.Orsi, G. B., L. Di Stefano, and N. Noah. 2002. Hospital-acquired, laboratory-confirmed bloodstream infection: increased hospital stay and direct costs. Infect. Control Hosp. Epidemiol. 23:190-197. [DOI] [PubMed] [Google Scholar]
  • 415.Osmundsen, P. E. 1982. Contact dermatitis to chlorhexidine. Contact Dermatitis 8:81-83. [DOI] [PubMed] [Google Scholar]
  • 416.Parienti, J. J., P. Thibon, R. Heller, Y. Le Roux, P. von Theobald, H. Bensadoun, A. Bouvet, F. Lemarchand, and X. Le Coutour. 2002. Hand-rubbing with an aqueous alcoholic solution vs traditional surgical hand-scrubbing and 30-day surgical site infection rates—a randomized equivalence study. JAMA 288:722-727. [DOI] [PubMed] [Google Scholar]
  • 417.Passaro, D. J., L. Waring, R. Armstrong, F. Bolding, B. Bouvier, J. Rosenberg, A. W. Reingold, M. McQuitty, S. M. Philpott, W. R. Jarvis, S. B. Werner, L. S. Tompkins, and D. J. Vugia. 1997. Postoperative Serratia marcescens wound infections traced to an out-of-hospital source. J. Infect. Dis. 175:992-995. [DOI] [PubMed] [Google Scholar]
  • 418.Patrick, D. R., G. Findon, and T. E. Miller. 1997. Residual moisture determines the level of touch-contact-associated bacterial transfer following hand washing. Epidemiol. Infect. 119:319-325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 419.Paulsen, D. S., E. J. Fendler, M. J. Dolan, and R. A. Williams. 1999. A close look at alcohol gel as an antimicrobial sanitizing agent. Am. J. Infect. Control 27:332-338. [DOI] [PubMed] [Google Scholar]
  • 420.Pegues, D. A., D. V. Schidlow, O. C. Tablan, L. A. Carson, N. C. Clark, and W. R. Jarvis. 1994. Possible nosocomial transmission of Pseudomonas cepacia in patients with cystic fibrosis. Arch. Pediatr. Adolesc. Med. 148:805-812. [DOI] [PubMed] [Google Scholar]
  • 421.Pelke, S., D. Ching, D. Easa, and M. E. Melish. 1994. Gowning does not affect colonization or infection rates in a neonatal intensive care unit. Arch. Pediatr. Adolesc. Med. 148:1016-1020. [DOI] [PubMed] [Google Scholar]
  • 422.Peltroche-Llacsahuanga, H., G. Haase, and R. Lutticken. 1998. Methicillin-resistente Staphylococcus aureus (MRSA)—Klinische Implikationen. Chirurg 69:801-805. [DOI] [PubMed] [Google Scholar]
  • 423.Pereira, L. J., G. M. Lee, and K. J. Wade. 1997. An evaluation of five protocols for surgical handwashing in relation to skin condition and microbial counts. J. Hosp. Infect. 36:49-65. [DOI] [PubMed] [Google Scholar]
  • 424.Perencevich, E. N., M. T. Wong, and A. D. Harris. 2001. National and regional assessment of the antibacterial soap market: a step toward determining the impact of prevalent antibacterial soaps. Am. J. Infect. Control 29:281-283. [DOI] [PubMed] [Google Scholar]
  • 425.Perrenoud, D., A. Bircher, T. Hunziker, H. Suter, L. Bruckner-Tuderman, J. Stager, W. Thurlimann, P. Schmid, A. Suard, and N. Hunziker. 1994. Frequency of sensitization to 13 common preservatives in Switzerland. Contact Dermatitis 30:276-279. [DOI] [PubMed] [Google Scholar]
  • 426.Pessoa-Silva, C. L., C. M. Toscano, B. M. Moreira, A. L. Santos, A. C. C. Frota, C. A. Solari, E. L. T. Amorim, M. G. S. Carvalbo, L. M. Teixeira, and W. R. Jarvis. 2002. Infection due to extended-spectrum β-lactamase-producing Salmonella enterica subsp. enterica serotype infants in a neonatal unit. J. Pediatr. 141:381-387. [DOI] [PubMed] [Google Scholar]
  • 427.Pether, J. V. S., and R. J. Gilbert. 1971. The survival of salmonellas on finger-tips and transfer of the organisms to foods. J. Hyg. (Cambridge) 69:673-681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 428.Pethica, B. 1958. Bacterial lysis: lysis by physical and chemical methods. J. Gen. Microbiol. 15:166-168. [DOI] [PubMed] [Google Scholar]
  • 429.Pettinger, A., and M. D. Nettleman. 1991. Epidemiology of isolation precautions. Infect. Control Hosp. Epidemiol. 12:303-307. [DOI] [PubMed] [Google Scholar]
  • 430.Pham, N. H., J. M. Weiner, G. S. Reisner, and B. A. Baldo. 2000. Anaphylaxis to chlorhexidine. Case report. Implication of immunoglobulin E antibodies and identification of an allergenic determinant. Clin. Exposure Allergy 30:1001-1007. [DOI] [PubMed] [Google Scholar]
  • 431.Piednoir, E., K. Bessaci, F. Bureau-Chalot, P. Sabouraud, V. Brodard, L. Andréoletti, and O. Bajolet. 2003. Economic impact of healthcare-associated rotavirus infection in a paediatric hospital. J. Hosp. Infect. 55:190-195. [DOI] [PubMed] [Google Scholar]
  • 432.Pietsch, H. 2001. Hand antiseptics: rubs versus scrubs, alcoholic solutions versus alcoholic gels. J. Hosp. Infect. 48:S33-S36. [DOI] [PubMed] [Google Scholar]
  • 433.Pirtle, E. C., and G. W. Beran. 1991. Virus survival in the environment. Rev. Sci. Tech. 10:733-748. [DOI] [PubMed] [Google Scholar]
  • 434.Pitt, T. L., M. A. Gaston, and P. N. Hoffman. 1983. In vitro susceptibility of hospital isolates of various bacterial genera to chlorhexidine. J. Hosp. Infect. 4:173-176. [DOI] [PubMed] [Google Scholar]
  • 435.Pittet, D. 2001. Compliance with hand disinfection and its impact on hospital-acquired infections. J. Hosp. Infect. 48:S40-S46. [DOI] [PubMed] [Google Scholar]
  • 436.Pittet, D. 2001. Improving adherence to hand hygiene practice: a multidisciplinary approach. Emerg. Infect. Dis. 7:234-240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 437.Pittet, D. 2000. Improving compliance with hand hygiene in hospitals. Infect. Control Hosp. Epidemiol. 21:381-386. [DOI] [PubMed] [Google Scholar]
  • 438.Pittet, D., S. Dharan, S. Touveneau, V. Sauvan, and T. V. Perneger. 1999. Bacterial contamination of the hands of hospital staff during routine patient care. Arch. Intern. Med. 159:821-826. [DOI] [PubMed] [Google Scholar]
  • 439.Pittet, D., S. Hugonnet, S. Harbarth, P. Monronga, V. Sauvan, S. Touveneau, and T. V. Perneger. 2000. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 356:1307-1312. [DOI] [PubMed] [Google Scholar]
  • 440.Pittet, D., D. Tarara, and R. P. Wenzel. 1994. Nosocomial bloodstream infection in critically ill patients. Excess length of stay, extra costs, and attributable mortality. JAMA 271:1598-1601. [DOI] [PubMed] [Google Scholar]
  • 441.Platt, J., and R. A. Bucknall. 1985. The disinfection of respiratory syncytial virus by isopropanol and a chlorhexidine-detergent handwash. J. Hosp. Infect. 6:89-94. [DOI] [PubMed] [Google Scholar]
  • 442.Podda, M., T. Zollner, M. Grundmann-Kollmann, R. Kaufman, and W. F. Boehncke. 1999. Allergic contact dermatitis from benzyl alcohol during topical antimycotic treatment. Contact Dermatitis 41:302-303. [DOI] [PubMed] [Google Scholar]
  • 443.Poole, K. 2002. Mechanisms of bacterial biocide and antibiotic resistance. J. Appl. Microbiol. 92:55S-64S. [PubMed] [Google Scholar]
  • 444.Post, W. E., and H. K. Nicoll. 1910. The comparative efficiency of some common germicides. JAMA 55:1635-1639. [Google Scholar]
  • 445.Powell, U. M. 1945. The antiseptic properties of isopropyl alcohol in relation to cold sterilization. J. Indiana State Med. Assoc. 38:303-304. [Google Scholar]
  • 446.Preston, G. A., E. L. Larson, and W. E. Stamm. 1981. The effect of private isolation rooms on patient care practices, colonization and infection in an intensive care unit. Am. J. Med. 70:641-645. [DOI] [PubMed] [Google Scholar]
  • 447.Price, P. B. 1938. The bacteriology of normal skin: a new quantitative test applied to a study of the bacterial flora and the disinfectant action of mechanical cleansing. J. Infect. Dis. 63:301-318. [Google Scholar]
  • 448.Price, P. B. 1939. Ethyl alcohol as a germicide. Arch. Surg. 38:528-542. [DOI] [PubMed] [Google Scholar]
  • 449.Prombo, M. P., and E. B. Tilden. 1950. Evaluation of disinfectants by tests in vivo. J. Dent. Res. 29:108-122. [DOI] [PubMed] [Google Scholar]
  • 450.Quraishi, Z. A., M. McGuckin, and F. X. Blais. 1984. Duration of handwashing in intensive care units: A descriptive study. Am. J. Infect. Control 11:83-87. [DOI] [PubMed] [Google Scholar]
  • 451.Raju, T. N. K., and C. Kobler. 1991. Improving handwashing habits in the newborn nurseries. Am. J. Med. Sci. 302:355-358. [DOI] [PubMed] [Google Scholar]
  • 452.Rangel-Frausto, M. S., A. K. Houston, M. J. Bale, C. Fu, and R. P. Wenzel. 1994. An experimental model for study of Candida survival and transmission in human volunteers. Eur. J. Clin. Microbiol. Infect. Dis. 13:590-595. [DOI] [PubMed] [Google Scholar]
  • 453.Räuchle, A. 1987. Triclosan, p. 527-545. In A. Kramer, W. Weuffen, A. P. Krasilnikow, D. Gröschel, E. Bulka, and D. Rehn (ed.), Handbuch der Antiseptik. Gustav Fischer, Stuttgart, Germany.
  • 454.Rayan, G. M., and D. J. Flourney. 1987. Microbiologic flora of human fingernails. J. Hand Surg. 12A:605-607. [DOI] [PubMed] [Google Scholar]
  • 455.Reboli, A. C., J. F. John, and A. H. Levkoff. 1989. Epidemic methicillin-gentamicin-resistant Staphylococcus aureus in a neonatal intensive care unit. Am. J. Dis. Child. 143:34-39. [DOI] [PubMed] [Google Scholar]
  • 456.Reed, S. 1975. An investigation of the possible transmission of rhinovirus colds through direct contact. J. Hyg. (London) 75:249-258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 457.Reed, S. E. 1975. Proceedings: rhinovirus contamination of the hands. J. Med. Microbiol. 8:Piv. [PubMed]
  • 458.Regös, J., and H. R. Hitz. 1974. Investigation on the mode of action of triclosan, a broad spectrum antimicrobial agent. Zentbla. Bakteriol. Mikrobiol. Hygiene I Abt. Orig. A 226:390-401. [PubMed] [Google Scholar]
  • 459.Regös, J., O. Zak, R. Solf, W. A. Vischer, and E. G. Weirich. 1979. Antimicrobial spectrum of triclosan, a broad-spectrum antimicrobial agent for topical application. Dermatologica 158:72-79. [DOI] [PubMed] [Google Scholar]
  • 460.Reilly, J., S. Twaddle, J. McIntosh, and L. Kean. 2001. An economic analysis of surgical wound infection. J. Hosp. Infect. 49:245-249. [DOI] [PubMed] [Google Scholar]
  • 461.Reinicke, E. A. 1894. Bakteriologische Untersuchungen über die Desinfektion der Hände. Zentbl. Gynäkol. 47:1189-1199. [Google Scholar]
  • 462.Reybrouck, G. 1983. Role of hands in the spread of nosocomial infections. J. Hosp. Infect. 4:103-110. [DOI] [PubMed] [Google Scholar]
  • 463.Richards, M. J., J. R. Edwards, D. H. Culver, and R. P. Gaynes. 1999. Nosocomial infections in medical intensive care units in the United States. National Nosocomial Infections Surveillance System. Crit. Care Med. 27:887-892. [DOI] [PubMed] [Google Scholar]
  • 464.Richards, R. M. E., and R. H. Cavill. 1979. Electron-microscope study of the effect of chlorhexidine on Pseudomonas aeruginosa. Microbios 26:85-93. [PubMed] [Google Scholar]
  • 465.Richards, R. M. E., and J. M. Richards. 1979. Pseudomonas cepacia resistance to antibacterials. J. Pharm. Sci. 68:1436-1438. [DOI] [PubMed] [Google Scholar]
  • 466.Rikimaru, T., M. Kondo, and K. Oizumi. 2000. Efficacy of common antiseptics against mycobacteria. Int. J. Tuberc. Lung Dis. 4:570-576. [PubMed] [Google Scholar]
  • 467.Robertson, M. H. 1972. Survival of S. typhimurium in floor dust: a possible reservoir of infection in institutions. Public Health 97:39-45. [DOI] [PubMed] [Google Scholar]
  • 468.Rosenberg, A., S. D. Alatary, and A. F. Peterson. 1976. Safety and efficacy of the antiseptic chlorhexidine gluconate. Surg. Gynecol. Obstet. 143:789-792. [PubMed] [Google Scholar]
  • 469.Ross, R. S., S. Viazov, T. Gross, F. Hofmann, H.-M. Seipp, and M. Roggendorf. 2000. Transmission of hepatitis C virus from a patient to an anesthesiologist assistant to five patients. N. Engl. J. Med. 343:1851-1854. [DOI] [PubMed] [Google Scholar]
  • 470.Rotter, M. 1990. Hygiene der Hände. Z. Gesamte Hyg. 36:77-79. [PubMed] [Google Scholar]
  • 471.Rotter, M., W. Koller, and G. Wewalka. 1981. Eignung von Chlorhexidinglukonat- und PVP-Jod-haltigen Präparationen zur Händedesinfektion. Hyg. Med. 6:425-430. [Google Scholar]
  • 472.Rotter, M., W. Koller, and G. Wewalka. 1980. Povidone-iodine and chlorhexidine gluconate detergents for disinfection of hands. J. Hosp. Infect. 1:149-158. [DOI] [PubMed] [Google Scholar]
  • 473.Rotter, M., and M. Skopec. 2003. Entwicklung der Händehygiene und die Bedeutung der Erkenntnisse von Ignaz Ph. Semmelweis, p. 1-27. In G. Kampf (ed.), Hände-Hygiene im Gesundheitswesen. Springer-Verlag KG, Berlin, Germany.
  • 474.Rotter, M. L. 2004. European norms in hand hygiene. J. Hosp. Infect. 56(Suppl. 2):S6-S9. [DOI] [PubMed] [Google Scholar]
  • 475.Rotter, M. L. 1999. Hand washing and hand disinfection, p. 1339-1355. In C. G. Mayhall (ed.), Hospital epidemiology and infection control, 2nd ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
  • 476.Rotter, M. L. 1984. Hygienic hand disinfection. Infect. Control 5:18-22. [DOI] [PubMed] [Google Scholar]
  • 477.Rotter, M. L. 1981. Povidone-iodine and chlorhexidine gluconate containing detergents for disinfection of hands. J. Hosp. Infect. 2:275-280. [DOI] [PubMed] [Google Scholar]
  • 478.Rotter, M. L., and W. Koller. 1991. A European test for the evaluation of the efficacy of procedures for the antiseptic handwash. Hyg. Med. 16:4-12. [Google Scholar]
  • 479.Rotter, M. L., and W. Koller. 1990. Surgical hand disinfection: Effect of sequential use of two chlorhexidine preparations. J. Hosp. Infect. 16:161-166. [DOI] [PubMed] [Google Scholar]
  • 480.Rotter, M. L., and W. Koller. 1992. Test models for hygienic handrub and hygienic handwash: the effects of two different contamination and sampling techniques. J. Hosp. Infect. 20:163-171. [DOI] [PubMed] [Google Scholar]
  • 481.Rotter, M. L., W. Koller, and R. Neumann. 1991. The influence of cosmetic additives on the acceptability of alcohol-based hand disinfectants. J. Hosp. Infect. 18:57-63. [DOI] [PubMed] [Google Scholar]
  • 482.Rotter, M. L., W. Koller, G. Wewalka, H. P. Werner, G. A. J. Ayliffe, and J. R. Babb. 1986. Evaluation of procedures for hygienic hand disinfection: controlled parallel experiments on the Vienna test model. J. Hyg. (London) 96:27-37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 483.Rotter, M. L., R. A. Simpson, and W. Koller. 1998. Surgical hand disinfection with alcohols at various concentrations: parallel experiments using the new proposed European standards methods. Infect. Control Hosp. Epidemiol. 19:778-781. [DOI] [PubMed] [Google Scholar]
  • 484.Rüden, H., F. Daschner, and M. Schumacher. 1995. Nosokomiale Infektionen in Deutschland: Erfassung und Prävention (NIDEP-Studie). 1. Prävalenz nosokomialer Infektionen; Qualitätssicherung in der Krankenhaushygiene, vol. 56. Nomos-Verlagsgesellschaft, Baden-Baden, Germany.
  • 485.Russell, A. D. 1986. Chlorhexidine: antibacterial action and bacterial resistance. Infection 14:212-215. [DOI] [PubMed] [Google Scholar]
  • 486.Russell, A. D. 1997. Plasmids and bacterial resistance to biocides. J. Appl. Microbiol. 83:155-165. [DOI] [PubMed] [Google Scholar]
  • 487.Russell, A. D., and M. J. Day. 1993. Antibacterial activity of chlorhexidine. J. Hosp. Infect. 25:229-238. [DOI] [PubMed] [Google Scholar]
  • 488.Ruuskanen, O. 1995. Respiratory syncytial virus—is it preventable? J. Hosp. Infect. 30:494-497. [DOI] [PubMed] [Google Scholar]
  • 489.Saint, S. 2000. Clinical and economic consequences of nosocomial catheter-related bacteriuria. Am. J. Infect. Control 28:68-75. [DOI] [PubMed] [Google Scholar]
  • 490.Samadi, A. R., M. I. Huq, and Q. S. Ahmed. 1983. Detection of rotavirus in handwashings of attendants of children with diarrhoea. Br. Med. J. 286:188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 491.Samore, M. H., L. Venkataraman, P. C. DeGirolami, R. D. Arbeit, and A. W. Karchmer. 1996. Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea. Am. J. Med. 100:32-40. [DOI] [PubMed] [Google Scholar]
  • 492.Sartor, C., V. Jacomo, C. Duvivier, H. Tissot-Dupont, R. Sambuc, and M. Drancourt. 2000. Nosocomial Serratia marcescens infections associated with extrinsic contamination of a liquid nonmedicated soap. Infect. Control Hosp. Epidemiol. 21:196-199. [DOI] [PubMed] [Google Scholar]
  • 493.Sartor, C., R. Sambuc, M. C. Bimar, C. Gulian, and P. De Micco. 1995. Prevalence surveys of nosocomial infections using a random method in Marseille hospitals. J. Hosp. Infect. 29:209-216. [DOI] [PubMed] [Google Scholar]
  • 494.Sasatsu, M., K. Shimizu, N. Noguchi, and M. Kono. 1993. Triclosan-resistant Staphylococcus aureus. Lancet 341:756. [DOI] [PubMed] [Google Scholar]
  • 495.Sattar, S., N. Lloyd-Evans, and V. S. Springthorpe. 1986. Institutional outbreaks of rotavirus diarrhoea: potential role of fomites and environmental surfaces as vehicles for virus transmission. J. Hyg. (Cambridge) 96:277-289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 496.Sattar, S. A., M. Abebe, A. J. Bueti, H. Jampani, J. Newman, and S. Hua. 2000. Activity of an alcohol-based hand gel against human adeno-, rhino-, and rotaviruses using the fingerpad method. Infect. Control Hosp. Epidemiol. 21:516-519. [DOI] [PubMed] [Google Scholar]
  • 497.Sattar, S. A., Y. G. Karim, V. S. Springthorpe, and C. M. Johnson-Lussenburg. 1987. Survival of human rhinovirus type 14 dried onto nonporous inanimate surfaces: effect of relative humidity and suspending medium. Can. J. Microbiol. 33:802-806. [DOI] [PubMed] [Google Scholar]
  • 498.Sattar, S. A., R. A. Raphael, H. Lochnan, and V. S. Springthorpe. 1983. Rotavirus inactivation by chemical disinfectants and antiseptics used in the hospital. Can. J. Microbiol. 29:1464-1469. [DOI] [PubMed] [Google Scholar]
  • 499.Sattar, S. A., V. S. Springthorpe, J. Tetro, R. Vashon, and B. Keswick. 2002. Hygienic hand antiseptics: should they not have activity and label claims against viruses? Am. J. Infect. Control 30:355-372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 500.Sawyer, R. G., D. P. Raymond, S. J. Pelletier, T. D. Crabtree, T. G. Gleason, and T. L. Pruett. 2001. Implications of 2,457 consecutive surgical infections entering the year 2000. Ann. Surg. 233:867-874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 501.Saxen, H., M. Virtanen, P. Carlson, K. Hoppu, M. Pohjavuori, M. Vaara, J. Vuopio-Varkila, and H. Peltola. 1995. Neonatal Candida parapsilosis outbreak with a high case fatality rate. Pediatr. Infect. Dis. J. 14:776-781. [DOI] [PubMed] [Google Scholar]
  • 502.Schaberg, D. R., D. H. Culver, and R. P. Gaynes. 1991. Major trends in the microbial etiology of nosocomial infections. Am. J. Med. 91:72S-75S. [DOI] [PubMed] [Google Scholar]
  • 503.Schmitz, F.-J., J. Verhoef, and A. C. Fluit. 1999. Prevalence of resistance to MLS antibiotics in 20 European university hospitals participating in the European SENTRY surveillance programme. J. Antimicrob. Chemother. 43:783-792. [DOI] [PubMed] [Google Scholar]
  • 504.Schürmann, W., and H. J. Eggers. 1983. Antiviral activity of an alcoholic hand disinfectant: comparison of the in vitro suspension test with the in vivo experiments on hands, and on individual fingertips. Antiviral Res. 3:25-41. [DOI] [PubMed] [Google Scholar]
  • 505.Schürmann, W., and H. J. Eggers. 1985. An experimental study on the epidemiology of enteroviruses: water and soap washing of poliovirus 1-contaminated hands, its effectiveness and kinetics. Med. Microbiol. Immunol. 174:221-236. [DOI] [PubMed] [Google Scholar]
  • 506.Schweizer, H. P. 2001. Triclosan: a widely used biocide and its links to antibiotics. FEMS Microbiol. Lett. 202:1-7. [DOI] [PubMed] [Google Scholar]
  • 507.Scopetti, F., G. Orefici, F. Biondi, and F. Benini. 1983. Staphylococcus aureus resistant to methicillin and gentamicin as a cause of outbreak of epidemic enteritis in a hospital. Boll. Ist. Sieroter. Milan 62:406-411. [PubMed] [Google Scholar]
  • 508.Scott, D., A. Barnes, M. Lister, and P. Arkell. 1991. An evaluation of the user acceptability of chlorhexidine handwash formulations. J. Hosp. Infect. 18(Suppl. B):51-55. [DOI] [PubMed] [Google Scholar]
  • 509.Scott, E., and S. F. Bloomfield. 1990. The survival and transfer of microbial contamination via cloths, hands and utensils. J. Appl. Bacteriol. 68:271-278. [DOI] [PubMed] [Google Scholar]
  • 510.Seto, W. H., D. Tsang, R. W. Yung, T. Y. Ching, T. K. Ng, M. Ho, L. M. Ho, and J. S. Peiris. 2003. Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS). Lancet 361:1519-1520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 511.Shaker, L. A., A. D. Russell, and J. R. Furr. 1986. Aspects of the action of chlorhexidine on bacterial spores. Int. J. Pharm. 34:51-56. [Google Scholar]
  • 512.Shahid, N. S., W. B. Greenough, A. R. Samadi, M. I. Huq, and N. Rahman. 1996. Hand washing with soap reduces diarhoea and spread of bacterial pathogens in a Bangladesh village. J. Diarrhoeal Dis. Res. 14:85-89. [PubMed] [Google Scholar]
  • 513.Shaker, L. A., J. R. Furr, and A. D. Russell. 1988. Mechanism of resistance of Bacillus subtilis spores to chlorhexidine. J. Appl. Bacteriol. 64:531-539. [DOI] [PubMed] [Google Scholar]
  • 514.Shamseldin el Shafie, S., W. Smith, and G. Donnelly. 1995. An outbreak of gentamicin-resistant Klebsiella pneumoniae in a neonatal ward. Cent. Eur. J. Public Health 3:129-131. [PubMed] [Google Scholar]
  • 515.Shay, D. K., S. A. Maloney, M. Montecalvo, S. N. Banerjee, G. P. Wormser, M. J. Ardulno, L. A. Bland, and W. R. Jarvis. 1995. Epidemiology and mortality risk of vancomycin-resistant enterococcal bloodstream infections. J. Infect. Dis. 172:993-1000. [DOI] [PubMed] [Google Scholar]
  • 516.Sheikh, W. 1981. Development and validation of a neutralizer system for in vitro evaluation of some antiseptics. Antimicrob. Agents Chemother. 19:429-434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 517.Shimizu, M., K. Okuzumi, A. Yoneyama, T. Kunisada, M. Araake, H. Ogawa, and S. Kimura. 2002. In vitro antiseptic susceptibility of clinical isolates from nosocomial infections. Dermatology 204:21-27. [DOI] [PubMed] [Google Scholar]
  • 518.Simmons, B., J. Bryant, K. Neiman, L. Spencer, and K. Arheart. 1990. The role of handwashing in prevention of endemic intensive care unit infections. Infect. Control Hosp. Epidemiol. 11:589-594. [DOI] [PubMed] [Google Scholar]
  • 519.Simor, A. E., M. Lee, M. Vearncombe, L. Jones-Paul, C. Barry, M. Gomez, J. S. Fish, R. C. Cartotto, R. Palmer, and M. Louie. 2002. An outbreak due to multiresistant Acinetobacter baumannii in a burn unit: risk factors for acquisition and management. Infect. Control Hosp. Epidemiol. 23:261-267. [DOI] [PubMed] [Google Scholar]
  • 520.Slater-Radosti, C., G. van Aller, R. Greenwood, R. Nicholas, P. M. Keller, W. E. deWolf, F. Fan, D. J. Payne, and D. D. Jaworski. 2001. Biochemical and genetic characterization of the action of triclosan on Staphylococcus aureus. J. Antimicrob. Chemother. 48:1-6. [DOI] [PubMed] [Google Scholar]
  • 521.Slaughter, S., M. K. Hayden, C. Nathan, T.-C. Hu, T. Rice, J. van Voorhis, M. Matushek, C. Franklin, and R. A. Weinstein. 1996. A comparison of the effect of universal use of gloves and gowns with that of glove use alone on acquisition of vancomycin-resistant enterococci in a medical intensive care unit. Ann. Intern. Med. 125:448-456. [DOI] [PubMed] [Google Scholar]
  • 522.Slight, P. H., J. M. Weber, J. M. Campos, and S. A. Plotkin. 1987. Oxacillin-resistant coagulase-negative staphylococcal carriage rates in neonatal intensive care nurses and non-patient care hospital personnel. Am. J. Infect. Control 15:29-32. [DOI] [PubMed] [Google Scholar]
  • 523.Smit, H. A., P. J. Coenraads, A. P. Lavrijsen, and J. P. Nater. 1992. Evaluation of a self-administered questionnaire on hand dermatitis. Contact Dermatitis 26:11-16. [DOI] [PubMed] [Google Scholar]
  • 524.Smith, C. R. 1947. Alcohol as a disinfectant against tubercle bacillus. Public Health Rep. 62:1285-1295. [PubMed] [Google Scholar]
  • 525.Smith, D. R., K. Ohmura, and Z. Yamagata. 2003. Prevalence and correlates of hand dermatitis among nurses in a Japanese teaching hospital. J. Epidemiol. 13:157-161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 526.Snellman, E., and T. Rantanen. 1999. Severe anaphylaxis after a chlorhexidine bath. J. Am. Acad. Dermatol. 40:771-772. [DOI] [PubMed] [Google Scholar]
  • 527.Snydman, D. R. 2003. Shifting patterns in the epidemiology of nosocomial Candida infections. Chest 123:500S-503S. [DOI] [PubMed] [Google Scholar]
  • 528.Soleto, L., M. Pirard, M. Boelaert, R. Peredo, R. Vargas, A. Gianella, and P. van der Stuyft. 2003. Incidence of surgical site infections and the validity of the National Nosocomial Infections Surveillance System risk index in a general surgical ward in Santa Cruz, Bolivia. Infect. Control Hosp. Epidemiol. 24:26-30. [DOI] [PubMed] [Google Scholar]
  • 529.Spire, B., F. Barre-Sinoussi, and L. Montagnier. 1984. Inactivation of lymphadenopathy associated virus by chemical disinfectants. Lancet ii:899-901. [DOI] [PubMed] [Google Scholar]
  • 530.Sproat, L. J., and T. J. Inglis. 1994. A multicentre survey of hand hygiene practice in intensive care units. J. Hosp. Infect. 26:137-148. [DOI] [PubMed] [Google Scholar]
  • 531.Stamm, W. E. 1991. Catheter-associated urinary tract infections: epidemiology, pathogenesis, and prevention. Am. J. Med. 91(Suppl. 3B):65S-71S. [DOI] [PubMed] [Google Scholar]
  • 532.Steinbrecher, E., D. Sohr, S. Hansen, A. Nassauer, F. Daschner, H. Rüden, and P. Gastmeier. 2002. Surveillance postoperative Wundinfektionen—Referenzdaten des Krankenhaus-Infektions-Surveillance-Systems (KISS). Chirurg 73:73-82. [DOI] [PubMed] [Google Scholar]
  • 533.Steinbrecher, E., D. Sohr, A. Nassauer, F. Daschner, H. Rüden, and P. Gastmeier. 2000. Die häufigsten Erreger bel Intensivpatienten mit noskomialen Infektionen. Chemother. J. 9:179-183. [Google Scholar]
  • 534.Steinmann, J., R. Nehrkorn, and A. Meyer. 1995. Two in vivo protocols for testing virucidal efficacy of handwashing and hand disinfection. Zentbl. Hyg. Umweltmed. 196:425-436. [PubMed] [Google Scholar]
  • 535.Steinmann, J., R. A. Nehrkorn, and E. Losche. 1990. Viruswirksamkeit der hygienischen Händedesinfektion. Hyg. Med. 15:7-14. [Google Scholar]
  • 536.Stickler, D. J. 1974. Chlorhexidine resistance in Proteus mirabilis. J. Clin. Pathol. 27:284-287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 537.Stickler, D. J., C. L. Clayton, and J. C. Chawla. 1987. The resistance of urinary tract pathogens to chlorhexidine bladder washouts. J. Hosp. Infect. 10:28-39. [DOI] [PubMed] [Google Scholar]
  • 538.Stickler, D. J., and B. Thomas. 1980. Antiseptic and antibiotic resistance in gram-negative bacteria causing urinary tract infections. J. Clin. Pathol. 33:288-296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 539.Stickler, D. J., and B. Thomas. 1976. Sensitivity of Providencia to antiseptics and disinfectants. J. Clin. Pathol. 29:815-823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 540.Stingeni, L., V. Lapomarda, and P. Lisi. 1995. Occupational hand dermatitis in hospital environments. Contact Dermatitis 33:172-176. [DOI] [PubMed] [Google Scholar]
  • 541.Strausbaugh, L. J., D. L. Sewell, T. T. Ward, M. A. Pfaller, T. Heitzman, and R. Tjoelker. 1994. High frequency of yeast carriage on hands of hospital personnel. J. Clin. Microbiol. 32:2299-2300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 542.Suh, H. K., Y. H. Jeon, J. S. Song, S. J. Hwang, and H. J. Cheong. 1998. A molecular epidemiologic study of methicillin-resistant Staphylococcus aureus infection in patients undergoing middle ear surgery. Eur. Arch. Otorhinolaryngol. 255:347-351. [DOI] [PubMed] [Google Scholar]
  • 543.Suller, M. T. E., and A. D. Russell. 2000. Triclosan and antibiotic resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 46:11-18. [DOI] [PubMed] [Google Scholar]
  • 544.Tainter, M. L., A. U. Throndson, and R. B. Beard. 1944. Chemical sterilization of instruments. J. Am. Dent. Assoc. 31:479-489. [Google Scholar]
  • 545.Tambe, S. M., L. Sampath, and S. M. Modak. 2001. In vitro evaluation of the risk of developing bacterial resistance to antiseptics and antibiotics used in medical devices. J. Antimicrob. Chemother. 47:589-598. [DOI] [PubMed] [Google Scholar]
  • 546.Tammelin, A., F. Klötz, A. Hambraeus, E. Stähle, and U. Ransjö. 2003. Nasal and hand carriage of Staphylococcus aureus in staff at a department for thoracic and cardiovascular surgery: endogenous or exogenous source? Infect. Control Hosp. Epidemiol. 24:686-689. [DOI] [PubMed] [Google Scholar]
  • 547.Tan, L., N. H. Nielsen, D. C. Young, and Z. Trizna. 2002. Use of antimicrobial agents in consumer products. Arch. Dermatol. 138:1082-1086. [DOI] [PubMed] [Google Scholar]
  • 548.Tanner, F. W., and F. L. Wilson. 1943. Germicidal action of aliphatic alcohols. Proc. Soc. Exp. Biol. Med. 52:138-140. [Google Scholar]
  • 549.Tattawasart, U., A. C. Hann, J.-Y. Maillard, J. R. Furr, and A. D. Russell. 2000. Cytological changes in chlorhexidine-resistant isolates of Pseudomonas stutzeri. J. Antimicrob. Chemother. 45:145-152. [DOI] [PubMed] [Google Scholar]
  • 550.Tattawasart, U., J.-Y. Maillard, J. R. Furr, and A. D. Russell. 1999. Development of resistance to chlorhexidine diacetate and cetylpyridinium chloride in Pseudomonas stutzeri and changes in antibiotic susceptibility. J. Hosp. Infect. 42:219-229. [DOI] [PubMed] [Google Scholar]
  • 551.Tattawasart, U., J.-Y. Maillard, J. R. Furr, and A. D. Russell. 2000. Outer membrane changes in Pseudomonas stutzeri resistant to chlorhexidine diacetate and cetylpyridinium chloride. Int. J. Antimicrob. Agents 16:233-238. [DOI] [PubMed] [Google Scholar]
  • 552.Taylor, L. S. 1978. An evaluation of handwashing techniques. Nurs. Times 74:54-55, 108-111. [PubMed] [Google Scholar]
  • 553.Tenorio, A. R., S. M. Badri, N. B. Sahgal, B. Hota, M. Matushek, M. K. Hayden, G. M. Trenholme, and R. A. Weinstein. 2001. Effectiveness of gloves in the prevention of hand carriage of vancomycin-resistant Enterococcus species by health care workers after patient care. Clin. Infect. Dis. 32:826-829. [DOI] [PubMed] [Google Scholar]
  • 554.Thomas, B., and D. J. Stickler. 1979: Chlorhexidine resistance and the lipids of Providencia stuartii. Microbios 24:141-150. [PubMed] [Google Scholar]
  • 555.Thomas, B., L. Sykes, and D. J. Stickler. 1978. Sensitivity of urine-grown cells of Providencia stuartii to antiseptics. J. Clin. Pathol. 31:929-932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 556.Thomas, L., J. Y. Maillard, R. J. Lambert, and A. D. Russell. 2000. Development of resistance to chlorhexidine diacetate in Pseudomonas aeruginosa and the effect of a “residual” concentration. J. Hosp. Infect. 46:297-303. [DOI] [PubMed] [Google Scholar]
  • 557.Thomas, S., M. Agarwal, and G. Mehta. 2001. Intraoperative glove perforation—single versus double gloving in protection against skin contamination. Postgrad. Med. J. 77:458-460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 558.Thompson, B. L., D. M. Dwyer, X. T. Ussery, S. Denman, P. Vacek, and B. Schwartz. 1997. Handwashing and glove use in a long-term-care facility. Infect. Control Hosp. Epidemiol. 18:97-103. [DOI] [PubMed] [Google Scholar]
  • 559.Tibballs, J. 1996. Teaching hospital mdeical staff to handwash. Med. J. Aust. 164:14-17. [DOI] [PubMed] [Google Scholar]
  • 560.Tierno, P. M. 1999. Efficacy of triclosan. Am. J. Infect. Control 27:71-72. [DOI] [PubMed] [Google Scholar]
  • 561.Tilley, F. W. 1942. An experimental study of the influence of temperature on the bactericidal activities of alcohols and phenols. J. Bacteriol. 43:521-525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 562.Tilley, F. W., and J. M. Schaffer. 1926. Relation between the chemical constitution and germicidal activity of the monohydric alcohols and phenols. J. Bacteriol. 12:303-309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 563.Torricelli, R., and B. Wüthrich. 1996. Life-threatening anaphylactic shock due to skin application of chlorhexidine. Clin. Exposure Allergy 26:112. [DOI] [PubMed] [Google Scholar]
  • 564.Traore, O., V. S. Springthorpe, and S. A. Sattar. 2002. A quantitative study of the survival of two species of Candida on porous and non-porous environmental surfaces and hands. J. Appl. Microbiol. 92:549-555. [DOI] [PubMed] [Google Scholar]
  • 565.Tupker, R. A. 1996. Detergents and cleaners, p. 71-76. In P. G. M. van der Valk and H. I. Maibach (ed.), The irritant contact dermatitis syndrome. CRC Press, Inc., Boca Raton, Fla.
  • 566.Tyler, R., G. A. J. Ayliffe, and C. Bradley. 1990. Virucidal activity of disinfecants: studies with the poliovirus. J. Hosp. Infect. 15:339-345. [DOI] [PubMed] [Google Scholar]
  • 567.Urban, E., A. Tusnadi, G. Terhes, and E. Nagy. 2002. Prevalence of gastrointestinal disease caused by Clostridium difficile in a university hospital in Hungary. J. Hosp. Infect. 51:175-178. [DOI] [PubMed] [Google Scholar]
  • 568.van Bueren, J., R. A. Simpson, P. Jacobs, and B. D. Cookson. 1994. Survival of human immunodeficiency virus in suspension and dried onto surfaces. J. Clin. Microbiol. 32:571-574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 569.van der Zwet, W. C., G. A. Parlevliet, P. H. Savelkoul, J. Stoof, A. M. Kaiser, A. M. van Furth, and C. M. Vandenbroucke-Grauls. 2000. Outbreak of Bacillus cereus infections in a neonatal intensive care unit traced to balloons used in manual ventilation. J. Clin. Microbiol. 38:4131-4136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 570.van Engelenburg, F. A. C., F. G. Terpstra, H. Schuitemaker, and W. R. Moorer. 2002. The virucidal spectrum of a high concentration alcohol mixture. J. Hosp. Infect. 51:121-125. [DOI] [PubMed] [Google Scholar]
  • 571.van Nierop, W. H., A. G. Duse, R. G. Stewart, Y. R. Bilgeri, and H. J. Koornhof. 1998. Molecular epidemiology of an outbreak of Enterobacter cloacae on the neonatal intensive care unit of a provincial hospital in Gauteng, South Africa. J. Clin. Microbiol. 36:3085-3087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 572.Vazquez, J. A., L. M. Dembry, V. Sanchez, M. A. Vazquez, J. D. Sobel, C. Dmuchowski, and M. J. Zervos. 1998. Nosocomial Candida glabrata colonization: an epidemiologic study. J. Clin. Microbiol. 36:421-426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 573.Vigeant, P., V. G. Loo, and C. Bertrand. 1998. An outbreak of Serratia marcescens infections related to contaminated chlorhexidine. Infect. Control Hosp. Epidemiol. 19:791-794. [DOI] [PubMed] [Google Scholar]
  • 574.Villari, P., M. Crispino, A. Slavadori, and A. Scarcella. 2001. Molecular epidemiology of an outbreak of Serratia marcescens in a neonatal intensive care unit. Infect. Control Hosp. Epidemiol. 22:630-634. [DOI] [PubMed] [Google Scholar]
  • 575.Vischer, W. A., and J. Regos. 1974. Antimicrobial spectrum of triclosan, a broad spectrum antimicrobial agent. Zentbl. Bakteriol. Mikrobiol. Hyg. 226:376-389. [PubMed] [Google Scholar]
  • 576.von Rheinbaben, F., S. Schunemann, T. Gross, and M. H. Wolff. 2000. Transmission of viruses via contact in a household setting: experiments using bacteriophage strain phiXI174 as a model virus. J. Hosp. Infect. 46:61-66. [DOI] [PubMed] [Google Scholar]
  • 577.Voss, A., and P. Goroncy-Bermes. 2000. Elimination and post-disinfection transmission of Staphylococcus aureus from experimentally contaminated hands. Infect. Control Hosp. Epidemiol. 21:106. [Google Scholar]
  • 578.Voss, A., D. Milatovic, C. Wallrauch-Schwarz, V. T. Rosdahl, and I. Braveny. 1994. Methicillin-resistant Staphylococcus aureus in Europe. Eur. J. Clin. Microbiol. Infect. Dis. 13:50-55. [DOI] [PubMed] [Google Scholar]
  • 579.Voss, A., and A. F. Widmer. 1997. No time for handwashing!? Handwashing versus alcoholic rub: can we afford 100% compliance? Infect. Control Hosp. Epidemiol. 18:205-208. [DOI] [PubMed] [Google Scholar]
  • 580.Vu-Thien, H., J. C. Darbord, and D. Moissenet. 1998. Investigation of an outbreak of wound infections due to Alcaligenes xylosoxidans transmitted by chlorhexidine in a burns unit. Eur. J. Clin. Microbiol. 17:724-726. [DOI] [PubMed] [Google Scholar]
  • 581.Wagenvoort, J. H., W. Sluijsman, and R. J. Penders. 2000. Better environmental survival of outbreak vs. sporadic MRSA isolates. J. Hosp. Infect. 45:231-234. [DOI] [PubMed] [Google Scholar]
  • 582.Wagenvoort, J. H. T., and R. J. R. Penders. 1997. Long-term in-vitro survival of an epidemic MRSA phage-group III-29 strain. J. Hosp. Infect. 35:322-325. [DOI] [PubMed] [Google Scholar]
  • 583.Wagner, M. B., N. B. da Silva, A. R. Vinciprova, A. B. Becker, L. M. Burtet, and A. J. Hall. 1997. Hospital-acquired infections among surgical patients in a Brazilian hospital. J. Hosp. Infect. 35:277-285. [DOI] [PubMed] [Google Scholar]
  • 584.Walker, E. M., and J. A. Lowes. 1985. An investigation into in vitro methods for the detection of chlorhexidine resistance. J. Hosp. Infect. 6:389-397. [DOI] [PubMed] [Google Scholar]
  • 585.Wallhäuser, K. H. 1995. Praxis der Sterilisation-Desinfektion-Konservierung-Keimidentifizierung-Betriebshygiene, 5th ed. Thieme, Stuttgart, Germany.
  • 586.Walsh, B., P. H. Blakemore, and Y. J. Drabu. 1987. The effect of handcream on the antibacterial activity of chlorhexidine gluconate. J. Hosp. Infect. 9:30-33. [DOI] [PubMed] [Google Scholar]
  • 587.Walter, C. W. 1965. Disinfection of hands. Am. J. Surg. 109:691-693. [DOI] [PubMed] [Google Scholar]
  • 588.Walters, T. H., J. R. Furr, and A. D. Russell. 1983. Antifungal action of chlorhexidine. Microbios 38:195-204. [Google Scholar]
  • 589.Wang, J.-T., S.-C. Chang, W.-J. Ko, Y.-Y. Chang, M.-L. Chen, H.-J. Pan, and K.-T. Luh. 2001. A hospital-acquired outbreak of methicillin-resistant Staphylococcus aureus infection initiated by a surgeon carrier. J. Hosp. Infect. 47:104-109. [DOI] [PubMed] [Google Scholar]
  • 590.Ward, R. L., D. R. Knowlton, and M. J. Pierce. 1984. Efficiency of rotavirus propagation in cell culture. J. Clin. Microbiol. 19:748-753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 591.Warren, R., K. D. Ertel, R. G. Bartolo, M. J. Levine, P. B. Bryant, and L. F. Wong. 1996. The influence of hard water (calcium) and surfactants on irritant contact dermatitis. Contact Dermatitis 35:337-343. [DOI] [PubMed] [Google Scholar]
  • 592.Watanakunakorn, C., C. Wang, and J. Hazy. 1998. An observational study of hand washing and infection control practices by healthcare workers. Infect. Control Hosp. Epidemiol. 19:858-860. [DOI] [PubMed] [Google Scholar]
  • 593.Weber, D. J., W. A. Rutala, G. P. Samsa, M. B. Wilson, and K. K. Hoffmann. 1992. Relative frequency of nosocomial pathogens at a university hospital during the decade 1980 to 1989. Am. J. Infect. Control 20:192-197. [DOI] [PubMed] [Google Scholar]
  • 594.Weber, D. J., E. Sickbert-Bennett, M. F. Gergen, and W. A. Rutala. 2003. Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands. JAMA 289:1274-1277. [DOI] [PubMed] [Google Scholar]
  • 595.Weber, S., L. A. Herwaldt, L. A. Mcnutt, P. Rhomberg, P. Vaudaux, M. A. Pfaller, and T. M. Perl. 2002. An outbreak of Staphylococcus aureus in a pediatric cardiothoracic surgery unit. Infect. Control Hosp. Epidemiol. 23:77-81. [DOI] [PubMed] [Google Scholar]
  • 596.Webster, C., K. J. Towner, and H. Humphreys. 2000. Survival of Acinetobacter on three clinically related inanimate surfaces. Infect. Control Hosp. Epidemiol. 21:246. [DOI] [PubMed] [Google Scholar]
  • 597.Webster, J., J. L. Faoagali, and D. Cartwright. 1994. Elimination of methicillin-resistant Staphylococcus aureus from a neonatal intensive care unit after hand washing with triclosan. J. Paediatr. Child Health 30:59-64. [DOI] [PubMed] [Google Scholar]
  • 598.Wendt, C., B. Dietze, E. Dietz, and H. Rüden. 1997. Survival of Acinetobacter baumannii on dry surfaces. J. Clin. Microbiol. 35:1394-1397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 599.Wendt, C., B. Wiesenthal, E. Dietz, and H. Rüden. 1998. Survival of vancomycin-resistant and vancomycin-susceptible enterococci on dry surfaces. J. Clin. Microbiol. 36:3734-3736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 600.Werner, H.-P., and C. Engelhardt. 1978. Problematik der lnaktivierung am Beispiel des in vitro-Tests. Hyg. Med. 3:326-330. [Google Scholar]
  • 601.Westergren, G., and C.-G. Emilson. 1980. In vitro development of chlorhexidine resistance in Streptococcus sanguis and its transmissibility by genetic transformation. Scand. J. Dent. Res. 88:236-243. [DOI] [PubMed] [Google Scholar]
  • 602.Weuffen, W., R. Hetmanek, and H. Berling. 1984. Beitrag zur Eliminierung von Sporen aus Ethanol, p. 246-247. In A. Kramer, H. Wigert, and B. Kemter (ed.), Aspekte der Prophylaxe und Bekämpfung des infektiösen Hospitalismus, vol. 8. Barth, Leipzig, Germany.
  • 603.Weuffen, W., and A. Kramer. 1970. Erprobung antimykotisch wirksamer Substanzen am Modell der experimentellen Hahnekammepidermophytie. 2. Mitteilung. Vergleich von Ergebnissen des Fungistase-, Fungizidie-, und Hahnekammepidermophytietests. Mykosen 13:39-44. [PubMed] [Google Scholar]
  • 604.Wewalka, G., M. Rotter, W. Koller, and G. Stanek. 1977. Wirkungsvergleich von 14 Verfahren zur hygienischen Händedesinfektion. Zentbl. Bakteriol. Mikrobiol. Hyg. I Abt. Orig. B 165:242-249. [PubMed] [Google Scholar]
  • 605.Whitehouse, J. D., D. Friedman, K. B. Kirkland, W. J. Richardson, and D. J. Sexton. 2002. The impact of surgical-site infections following orthopedic surgery at a community hospital and a university hospital: adverse quality of life, excess length of stay, and extra costs. Infect. Control Hosp. Epidemiol. 23:183-189. [DOI] [PubMed] [Google Scholar]
  • 606.Widmer, A. F. 2000. Replace hand washing with use of a waterless alcohol hand rub? Clin. Infect. Dis. 31:136-143. [DOI] [PubMed] [Google Scholar]
  • 607.Widmer, A. F., R. P. Wenzel, A. Trilla, M. J. Bale, R. N. Jones, and B. N. Doebbeling. 1993. Outbreak of Pseudomonas aeruginosa infections in a surgical intensive care unit: probable transmission via hands of a health care worker. Clin. Infect. Dis. 16:372-376. [DOI] [PubMed] [Google Scholar]
  • 608.Williams, J. V., B. Vowels, P. Honig, and J. J. Leyden. 1999. Staphylococcus aureus isolation from the lesions, the hands, and anterior nares of patients with atopic dermatitis. J. Emerg. Med. 17:207-211. [DOI] [PubMed] [Google Scholar]
  • 609.Williams, J. V., B. R. Vowels, P. J. Honig, and J. J. Leyden. 1998. S. aureus isolation from the lesions, the hands, and the anterior nares of patients with atopic dermatitis. Pediatr. Dermatol. 15:194-198. [DOI] [PubMed] [Google Scholar]
  • 610.Wingard, E., J. H. Shlaes, E. A. Mortimer, and D. M. Shlaes. 1993. Colonization and cross-colonization of nursing home patients with trimethoprim-resistant gram-negative bacilli. Clin. Infect. Dis. 16:75-81. [DOI] [PubMed] [Google Scholar]
  • 611.Winnefeld, M., M. A. Richard, M. Drancourt, and J. J. Grobb. 2000. Skin tolerance and effectiveness of two hand decontamination procedures in everyday hospital use. Br. J. Dermatol. 143:546-550. [DOI] [PubMed] [Google Scholar]
  • 612.Wirgin, G. 1904. Vergleichende Untersuchungen über die keimabtötenden und die entwicklungshemmenden Wirkungen von Alkoholen der Methyl-, Äthyl-, Propyl-, Butyl-, und Amylreihen. Z. Hyg. 46:49-168. [Google Scholar]
  • 613.Wistrom, J., S. R. Norrby, E. B. Myhre, S. Eriksson, G. Granstrom, L. Lagergren, G. Englund, C. E. Nord, and B. Svenungsson. 2001. Frequency of antibiotic-associated diarrhoea in 2462 antibiotic-treated hospitalized patients: a prospective study. J. Antimicrob. Chemother. 47:43-50. [DOI] [PubMed] [Google Scholar]
  • 614.Wladowetz, V. W., R. A. Dmitrijewa, and A. A. Safjulin. 1974. Die Persistenz von Viren auf Oberflächen und die Anwendung der UV-Bestrahlung zur Virusdesinfektion. Z. Gesamte Hyg. 7:173-176. [PubMed] [Google Scholar]
  • 615.Wolff, M. H., J. Schmitt, M. Rahaus, and A. König. 2001. Hepatitis A virus: a test method for virucidal activity. J. Hosp. Infect. 48:S18-S22. [DOI] [PubMed] [Google Scholar]
  • 616.Wong, C. S. M., and M. H. Beck. 2001. Allergic contact dermatitis from triclosan in antibacterial handwashes. Contact Dermatitis 45:307. [DOI] [PubMed] [Google Scholar]
  • 617.Wong, W. K., C. L. Goh, and K. W. Chan. 1990. Contact urticaria from chlorhexidine. Contact Dermatitis 22:52. [DOI] [PubMed] [Google Scholar]
  • 618.Wurtz, R., G. Moye, and B. Jovanovic. 1994. Handwashing machines, handwashing compliance, and potential for cross-contamination. Am. J. Infect. Control 22:228-230. [DOI] [PubMed] [Google Scholar]
  • 619.Yamamoto, T., Y. Tamura, and T. Yokota. 1988. Antiseptic and antibiotic resistance plasmid in Staphylococcus aureus that possesses ability to confer chlorhexidine and acrinol resistance. Antimicrob. Agents Chemother. 32:932-935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 620.Yesudian, P. D., and C. M. King. 2001. Allergic contact dermatitis from stearyl alcohol in efudix cream. Contact Dermatitis 45:313-314. [DOI] [PubMed] [Google Scholar]
  • 621.Zafar, A. B., R. C. Butler, D. J. Reese, L. A. Gaydos, and P. A. Mennonna. 1995. Use of 0.3% triclosan (Baoti-Stat*) to eradicate an outbreak of methicillin-resistant Staphylococcus aureus in a neonatal nursery. Am. J. Infect. Control 23:200-208. [DOI] [PubMed] [Google Scholar]
  • 622.Zimakoff, J., M. Stormark, and S. Olesen Larsen. 1993. Use of gloves and handwashing behaviour among health care workers in intensive care units. A multicentre investigation in four hospitals in Denmark and Norway. J. Hosp. Infect. 24:63-67. [DOI] [PubMed] [Google Scholar]
  • 623.Zyzik, E., W. H. Gerlich, A. Uy, H. Kochel, and R. Thomssen. 1986. Assay of hepatitis B virus genome titers in sera of infected subjects. Eur. J. Clin. Microbiol. 5:330-335. [DOI] [PubMed] [Google Scholar]

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